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Phylogenetic generic classification of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological and chemical evidence

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  • Complutense University of Madrid, Faculty of Pharmacy

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Parmelioid lichens are a diverse and ubiquitous group of foliose lichens. Generic delimitation in parmelioid lichens has been in a state of flux since the late 1960s with the segregation of the large, heterogeneous genus Parmelia into numerous smaller genera. Recent molecular phylogenetic studies have demonstrated that some of these new genera were monophyletic, some were not, and others, previously believed to be unrelated, fell within single monophyletic groups, indicating the need for a revision of the generic delimitations. This study aims to give an overview of current knowledge of the major clades of all parmelioid lichens. For this, we assembled a dataset of 762 specimens, including 31 of 33 currently accepted parmelioid genera (and 63 of 84 accepted genera of Parmeliaceae). We performed maximum likelihood and Bayesian analyses of combined datasets including two, three and four loci. Based on these phylogenies and the correlation of morphological and chemical characters that characterize monophyletic groups, we accept 27 genera within nine main clades. We re-circumscribe several genera and reduce Parmelaria to synonymy with Parmotrema. Emodomelanelia Divakar & A. Crespo is described as a new genus (type: E. masonii). Nipponoparmelia (Kurok.) K.H. Moon, Y. Ohmura & Kashiw. ex A. Crespo & al. is elevated to generic rank and 15 new combinations are proposed (in the genera Flavoparmelia, Parmotrema, Myelochroa, Melanelixia and Nipponoparmelia). A short discussion of the accepted genera is provided and remaining challenges and areas requiring additional taxon sampling are identified.
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Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
Phylogenetic generic classification of parmelioid lichens (Parmeliaceae,
Ascomycota) based on molecular, morphological and chemical evidence
Ana Crespo,1 Frank Kauff,2 Pradeep K. Divakar,1 Ruth del Prado,1 Sergio Pérez-Ortega,1
Guillermo Amo de Paz,1 Zuzana Ferencova,1 Oscar Blanco,3 Beatriz Roca-Valiente,1 Jano Núñez-Zapata,1
Paloma Cubas,1 Arturo Argüello,1 John A. Elix,4 Theodore L. Esslinger,5 David L . Hawksworth,1
Ana Millanes,6 M. Carmen Molina,6 Ma t s Wedin,7 Teuvo Ahti,8 Andre Aptroot,9 Eva Barreno,10
Frank Bungartz,11 Susana Calvelo,12 Mehmet Candan,13 Mariette Cole,14 Damien Ertz,15 Bernard Goffinet,16
Louise Lindblom,17 Robert Lücking,18 Francois Lutzoni,19 Jan-Eric Mattsson,20 María Inés Messuti,11
Jolanta Miadlikowska,19 Michele Piercey-Normore,21 Víctor J. Rico,1 Harrie J.M. Sipman,22 Imke Schmitt,23
Toby Spribille,24 Arne Thell,25 Göran Thor,26 Dalip K. Upreti27 & H. Thorsten Lumbsch18
1 Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Plaza de Ramón y Cajal s/n,
28040 Madrid, Spain
2 FB Biologie, Molecular Phylogenetics, 13/276, TU Kaiserslautern, Postfach 3049, 67653 Kaiserslautern, Germany
3 Unidad de Bioanálisis, Centro de Investigación y Control de calidad, Instituto Nacional del Consumo, Avda Cantabria s/n 28042
Madrid, Spain
4 Department of Chemistry, Australian National University, P.O. Box 4, Canberra, A.C.T. 0200, Australia
5 Department of Biological Sciences Dept. 2715, PO Box 6050, North Dakota State University, Fargo, North Dakota 58108-6050, U.S.A.
6 Área de Biodiversidad y Conservación, Universidad Rey Juan Carlos, c/ Tulipán s/n., 28933 Móstoles (Madrid), Spain
7 Cryptogamic Botany, Swedish Museum of Natural History, P.O. Box 50007, 104 05 Stockholm, Sweden
8 Botanical Garden and Museum, Finnish Museum of Natural History, P.O. Box 7, 00014 Helsinki University, Finland
9 ABL Herb arium, G. v. d. Veenstraat 107, 3762 XK, Soest, Netherlands
10 Department of Botany, Fac. of Biology, Universitat de València, ICBIBE, C/ Dr. Moliner 50, 46100 Burjassot (Valencia), Spain
11 Charles Darwin Foundation for the Galapagos Islands, Av. 6 de Diciembre N 36-109 y Pasaje California, Post Box 17-01-3891,
Quito, Ecuador
12 Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA, CONICET-UNComahue), Quintral 1250, R8400 FRF,
San Carlos de Bariloche, Río Negro, Argentina
13 Department of Biology, Faculty of Science, Anadolu University, Esk işehir, Turkey
14 2017 Thure Ave., St. Paul, Minnesota 55116, U.S.A.
15 Department of Bryophytes-Thallophytes, Domaine de Bouchout, National Botanic Garden of Belgium, 1860 Meise, Belgium
16 Ecology and Evolutionary Biology, 75 North Eagleville Road, University of Connecticut, Storrs, Connecticut 06269-3043, U.S.A.
17 Museum of Natural History, University of Bergen, Box 7800, 5020, Bergen, Norway
18 Department of Botany, The Field Museum, 1400 S. Lake Shore Drive, Chicago, Illinois 60605, U.S.A.
19 Department of Biology, Duke University, Box 90338, Durham, North Carolina 27708, U.S.A.
20 School of Life Sciences, Södertörns University, 141 89 Huddinge, Sweden
21 Department of Botany, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada
22 Botanischer Garten und Botanisches Museum Berlin-Dahlem, Freie Universität Berlin, Königin-Luise-Straße 6– 8, 14195 Berlin,
Germany
23 Biodiversity and Climate Research Centre BiK-F, Senckenberganlage 25, 60325 Frankfurt am Main, Germany
24 Institute for Plant Sciences, Karl-Franzens-University Graz, Holteigasse 6, 8010 Graz, Austria
25 Lund University, Dept. of Systematic Botany, Östra Vallgatan 18–20, 223 61 Lund, Sweden
26 Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, 750 07 Uppsala, Sweden
27 National Botanical Research Institute (CSIR), Rana Pratap Marg, Lucknow-226001, Uttar Pradesh, India
Author for correspondence: H. Thorsten Lumbsch, tlumbsch@fieldmuseum.org
Abstract
Parmelioid lichens are a diverse and ubiquitous group of foliose lichens. Generic delimitation in parmelioid lichens
has been in a state of flux since the late 1960s with the segregation of the large, heterogeneous genus Parmelia into numerous
smaller genera. Recent molecular phylogenetic studies have demonstrated that some of these new genera were monophyletic,
some were not, and others, previously believed to be un related, fell within single monophyletic groups, indicating the need
for a revision of the generic delimitations. This study aims to give an overview of current knowledge of the major clades of
all parmelioid lichens. For this, we assembled a dataset of 762 specimens, including 31 of 33 currently accepted par melioid
genera (and 63 of 84 accepted genera of Parmeliaceae). We performed maximum likelihood and Bayesian analyses of combined
datasets including t wo, three and four loci. Based on these phylogenies and the correlation of morphological and chemical
Ta xo n o my
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TA XO N 59 (6) • December 2010: 1735–1753Crespo & al. • Generic classification of parmelioid lichens
INTRODUCTION
The delimitation of genera in lichen-forming fungi has been
in a state of flux since the late 1960s (Poelt, 1966; Hale, 1984b;
Elix, 1993; Nimis, 1998; DePriest, 1999) with parmelioid lichens
being a prominent example of this. No other group of lichenized
ascomycetes was the subject of such vigorous and controversial
debates about the recognition and circumscription of genera
than these common foliose lichens. Parmelioid lichens have
mostly foliose, dorsiventral thalli, usually with rhizines on the
lower surface, laminal pycnidia and apothecia, Lecanora-type
asci and simple hyaline ascospores (Crespo & al., 2001, 2007).
With the exception of one study (Thell & al., 2004) that had
parmelioid lichens fall into two separate groups, phylogenetic
studies converged on one monophyletic core group of parmeli-
oid genera (Crespo & al., 2001, 2007; Blanco & al., 2006). Par-
melioid lichens represent the largest group within Parmeliaceae,
including about 75% of the described species in this family,
which is among the largest families of lichen-forming fungi with
nearly 2500 species (Kirk & al., 2008). The parmelioid group
comprises common and well-known species, such as Parmelia
sulcata, Flavoparmelia caperata, Parmotrema perlatum, and
Punctelia subrudecta, which are frequently used in biomonitor-
in g studies of atmo sphe r ic pollution (Cre spo & al., 1999b, 200 4;
Nimis & al., 2002). Besides the typical foliose growth forms,
some genera with deviating morphologies, such as the peltate
Omphalodiella, subcrustose Karoowia, subfruticose Almbornia
and umbilicate Xanthomaculina have been shown to belong to
the parmelioid lichens (Esslinger, 1981; Hale, 1985, 1989; Hens-
sen, 1991; Thell & al., 2006). Recent molecular studies added
Parmeliopsis, Cetrelia and Parmelaria ( prev io usly re cog n ized
as cetrarioid lichens), and even the lichenicolous fungus Ne-
solechia, to the parmelioid clade (Peršoh & Rambold, 2002;
Blanco & al., 2004a, 2005; Crespo & al., 2007). As taxa were
added to the parmelioid clade, taxa that were seen as typical
parmelioid lichens, such as Allantoparmelia, Arctoparmelia,
Melanelia s.st r., and Psiloparmelia, have been found to belong
to non-parmelioid groups (Crespo & al., 2007).
Traditional generic classification within parmelioid lichens
has relied mostly on morphological and chemical characters
of the thallus (Hale, 1974, 1984a, 1986a,b, 1988; Elix & Hale,
1987; Elix, 1993; Crespo & al., 1999a; Divakar & Upreti,
2005a). Acceptance of new genera, segregated from established
genera of parmelioid lichens in the absence of ascomatal char-
acters has not been uniform (Poelt & Vězda, 1981; Clauzade &
Roux, 1986; Eriksson & Hawk s wo r t h , 1986; Pu rvis & al., 1992;
Llimona & Hladu n, 20 01). Ba sed on the late Mason Ha le’s 30-
year study of Parmeliaceae, DePriest (1999) gave an overview
of his generic delimitation of parmelioid lichens. Hale recog-
nized 36 genera in this group. Subsequently, some of these
genera were included within other genera based on morpho-
logical and/or molecular evidence. These include Rimeliella,
which was placed into synonymy with Canomaculina (Elix,
1997); Almbornia, Chondropsis, Namakwa, Paraparmelia,
Neofuscelia, and Xanthomaculina, which were included in Xan-
thoparmelia (Hawksworth & Crespo, 2002; Elix, 2003; Blanco
& al., 2004b; Thell & al., 2006); and Canomaculina, Conca-
merella, and Rimelia, which were merged with Parmotrema
(Blanco & al., 2005). Recently, two additional generic names
(Omphalodiella, Placoparmelia) were added as synonyms of
Xanthoparmelia (Amo & al., 2010a) and Karoowia was shown
to be highly polyphyletic and nested within Xanthoparmelia
as well (Amo & al., 2010b). Other genera were found to be
polyphyletic, such as Melanelia (Blanco & al., 2004a), which
fell into four distinct clades, two of which were recognized as
new genera (Melanelixia and Melanohalea). Hypotrachyna
provides another example, with Cetrariastrum, Everniastrum
and Parmelinopsis clustered within a core group of Hypotra-
chyna, whereas a second group of Hypotrachyna formed a
sister clade with Bulbothrix and Parmelinella (Divakar & al.,
2006). The latter Hypotrachyna clade was subsequently seg-
regated as Remototrachyna (Divakar & al., 2010). Similarly,
an Australasian clade of Parmelina was described as a new
genusAustroparmelina (Crespo & al., 2010).
Although several studies have addressed generic delimita-
tions of parmelioid lichens, the scope of these studies was limited
to smaller groups of genera. With the exception of a checklist of
European species (Hawksworth & al., 2008), a modern synthesis
of the generic classification of parmelioid lichens, summarizing
results from molecular phylogenetic studies is still lacking. To
fill this gap, we initiated a collaborative research project (PAR-
SYS, parmelioid systematics) to assemble the largest and most
inclusive dataset of DNA sequences of parmelioid lichens to date
to address the generic classification within this group.
Specifically, this study aimed at: (1) elucidating evolution-
ary relationships among parmelioid lichens with phylogenetic
characters that characterize monophyletic groups, we accept 27 genera within nine main clades. We re-circumscribe several
genera and reduce Parmelaria to synony my with Parmotrema. Emodomelanelia Divakar & A. Crespo is described as a new
genus (type: E. masonii). Nipponoparmelia (Kurok.) K.H. Moon, Y. Ohmura & Kashiw. ex A. Crespo & al. is elevated to
generic rank and 15 new combinations are proposed (in the genera Flavoparmelia, Parmotrema, Myelochroa, Melanelixia
and Nipponoparmelia). A short discussion of the accepted genera is provided and remaining challenges and areas requiring
additional taxon sampling are identified.
Keywords
combined analysis; Emodomelanelia; generic concept; Lecanorales; large-scale phylogeny; lichens; lichenized
fungi; Nipponoparmelia; Parmeliaceae; Parmotrema; taxonomy
Supplementary Material
Figures S1–S2 and the Appendix are available in the free Electronic Supplement to the online
version of this article (ht tp://www.ingentaconnect.com/content/iapt/tax).
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Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
analyses of a four-locus (the nuclear RPB1 protein-coding gene,
and the nuclear ITS, nuclear LSU, and mitochondrial SSU
rDNA) dataset including 762 samples representing 470 spe-
cies including almost all currently accepted genera; (2) provid-
ing a comprehensive and coherent classification at the generic
level for parmelioid lichens reflecting current knowledge of
phylogenetic relationships and giving a short morphological
and chemical characterization of monophyletic genera; and (3)
identifying generic groups that need additional molecular and
morphological work before taxonomic changes can be proposed.
MATERIALS AND METHODS
Molecular methods. —
Samples prepared from freshly
collected, frozen samples or herbarium specimens were ground
with sterile glass pestles. Total genomic DNA was extracted us-
ing the DNeasy Plant Mini Kit (Qiagen) according to the manu-
facturer’s instructions and 1–25 ng genomic DNA was used
for PCR amplifications of the inte r nal tran scr ibed spacer (ITS)
and the genes coding for the nuclear LSU rRNA, mitochondrial
SSU and the protein-coding R PB1 gene, respectively. Prim-
ers for amplification were: (i) for the nuclear LSU rDNA: nu-
LSU-0155–5′ (Döring & al., 2000), nu-LSU-0042–5′ (= LR0R)
(Vilgalys, unpub., http://www.botany.duke.edu/fungi/mycolab),
AL2R (Mangold & al., 2008), nu-LSU-1432–3′ (= LR7), LR5
and nu-LSU-1125–3′ (= LR6) (Vilgalys & Hester, 1990); (ii) for
the nuclear ITS rDNA: ITS1F (Gardes & Bruns, 1993), ITS4
(W hite & al., 199 0) and ITS1-LM (Myl lys & al., 1999) an d ITS2-
KL (Lohtander & al., 1998); (iii) for the mitochondrial SSU
rDNA: mrSSU1 and mrSSU3R (Zoller & al., 1999), and MSU
7 (Zhou & Stanosz, 2001), and (iv) for RPB1 nuDNA: gR PB1-A
(Stiller & Hall, 1997) and fRPB1-C (Matheny & al., 2002), and
RPr2 (Wirtz & al., 2008). The 25 µL PCR reactions contained
1× buffer (containing 10 mM Tris pH 9.0, 2.5 mM MgCl2, 50
mM KCl, 0.1% TritonX-100), 0.2 mM each dN TP, 0.5 µM each
primer, 1.25 units Taq DNA polymerase (Applied Biosystems)
and 1–10 ng genomic DNA extract. Alternatively, amplifica-
tions were performed in 50 µL volumes containing a reaction
mixture of 5–25 ng genomic DNA, 1× DNA polymerase buffer
(Biotools) (containing 2 mM MgCl2, 10 mM Tris-HCl pH 8.0,
50 mM KCl, 1 mM EDTA, 0.1% Triton X-100), 0.2 mM each
dNTP, 0.5 µM each primer and 1.25 units DNA polymerase
(Biotools). PCRs on some samples were performed using Amer-
sham Pharmacia Biotech Ready-To-Go Beads. Thermal cycling
parameters were: initial denaturation for 3 min at 95°C, followed
by 30 cycles of 1 min at 95°C, 1 min at 52°C, 1 min at 73°C, and
a f inal elongation for 7 min at 73°C. Amplif ications of some
samples were carried out in a Techne Progene thermocycler and
performed using the following programs: initial denaturation at
94°C for 5 min, and 30 cycles of: 94°C for 1 min, 54°C–60°C
(ITS nrDNA), 60°C (LSU nrDNA), 57°C–58°C (SSU mtrDNA)
and 52°C (RPB1 nrDNA) for 1 min, 72°C for 1.5 mi n , and a fina l
extension at 72°C for 5 min.
Amplification products were viewed on 1% agarose gels
stained with ethidium bromide and subsequently purified us-
ing the QIAquick PCR Purification Kit (Qiagen) and DNA
Purification Column kit (Biotools) according to the manufac-
turer’s instructions. The cleaned PCR products were sequenced
using the same primers used in the amplifications. The ABI
Prism™ Dye Terminator Cycle Sequencing Ready reaction kit
(Applied Biosystems) was used with the following settings:
denaturation for 3 min at 94°C and 25 cycles at: 96°C for 10 s,
50°C for 5 s and 60°C for 4 min. Sequencing reactions were
elec t rophore sed on a 3730 DNA an aly ser (Applied Biosy stem s).
Sequence fragments obtained were assembled with SeqMan
v.4.03 (DNAStar) and manually adjusted.
Taxon sampling. —
Data collec tion ac ross al l par t icipant s
of the PARSYS project was facilitated using a web site (Zope
2.10.4) and an SQL database (Postgresql 8.2.4). Sequences
which were newly generated for PARSYS were complemented
with sequence data from GenBank (www.ncbi.nlm.nih.gov), us-
ing several scripts in the Python programming language (www
.python.org) with modules provided from Biopython (Cock
& al., 2009) to download and filter the available data. First,
all available sequences belonging to Parmeliaceae and the ge-
nus Phacopsis (according to NCBI’s taxonomy browser), plus
sequences from the genus Protoparmelia as outgroup, were
downloaded from GenBank. The choice of outgroup follows
Crespo & al. (2007). Second, the downloaded data were filtered
for sequences belonging to the nuclear ribosomal large subunit
(nucLSU), the nuclear ribosomal intergenic spacers (nucITS,
including the 5.8S rDNA), the mitochondrial ribosomal small
subunit (mitSSU), and the largest subunit of the RNA poly-
merase II (RPB1). Other available gene loci were discarded due
to insufficient data. Initial alignments were created with Clust-
alW (Thompson & al., 1994) and optimized manually using
Seaview (Galtier & al., 1996). Mislabeled or otherwise unalign-
able sequences were removed during the process. Introns and
ambiguously aligned regions were excluded prior to all analyses.
Dataset assembly. —
The initial datasets for each locus
were created by selecting from the initial alignments a maxi-
mu m of two seq uences per species. If mor e than two sequenc es
were available for a given species, the longer sequences were
given priority. As a consequence, the resulting single-locus
datasets (1GENE, 762 OTUs) contained sequences from all
species for which sequence information was available, but with
no more than two OTUs per species. For a complete list of
sequences see Appendix.
For the phylogenetic analysis of the combined data, three
datasets were generated from the 1GENE single locus datasets by
combining only those specimens for which sequence data from
at least two (2GENE, 433 OTUs), at least three (3GENE, 323
OTUs), or all four (4GENE, 145 OTUs) loci per specimen was
present, following the strategy of Miadlikowska & al. (2006).
Test for incongruence.
The 1GENE single locus data-
sets were used to test for topological incongruence among loci
using the program compat3 (available at www.lutzonilab.net/
downloads). For each locus individually, 500 bootstrap repli-
cates (Felsenstein, 1985) were generated with RAxML v.7.0.4
(Stamatakis, 2006, Stamatakis & al., 2008) and all pairwise
comparisons between the four loci were performed with com-
pat3. A conf lict between two loci was assumed when a clade
was supported as monophyletic with a bootstrap frequency
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TA XO N 59 (6) • December 2010: 1735–1753Crespo & al. • Generic classification of parmelioid lichens
≥75% in one tree, but supported as non-monophyletic in another
(Mason-Gamer & Kellogg, 1996).
Phylogenetic analyses. —
Phylogenetic searches were
carried out by implementing maximum likelihood (ML) and
Bayesian analyses on each of the three combined datasets
(2GENE, 3GENE, and 4GENE). The analyses were run on
the Duke Shared Cluster Resource (DSCR, Duke University,
U.S.A.) and the computer cluster of the Nano+Bio Center (Uni-
versity of Kaiserslautern, Germany). If not stated otherwise,
all three datasets were analyzed in the same way.
For one set of ML analyses the 2GENE, 3GENE and
4GENE combined datasets were partitioned into eight parti-
tions: nucLSU, mitSSU, nucITS1, nuc5.8S, nucITS2, RPB1 1st
position, R PB1 2nd position, and RPB1 3rd position. The ML
analyses were carried out using RAxML v.7.0.4 (Stamatakis,
2006), implementing a GTR model of nucleotide substitution
(Rodriguez & al., 1990) with a gamma shape distribution, and
searching for the most likely tree with 500 heuristic replicates.
Bootstrap frequencies (Felsenstein, 1985; Stamatakis & al.,
2008) were estimated with 500 replicates.
The second set of ML analyses was implemented with
GARLI v.0.96 (Zwickl, 2006). The 2GENE, 3GENE, and
4GENE datasets were analyzed unpartitioned, because GARLI
currently does not support multiple partitions. Tree search was
performed with 500 replicates using the standard settings of
GARLI, implementing a GTR model of nucleotide substitution
with a gamma shape distribution (approximated with four cat-
egories), and a proportion of invariable sites. Bootstrap frequen-
cies were estimated with 500 replicates, limiting the parameter
‘genthreshfortopoterm’ to 10,000 generations, as suggested in
the manual.
In the Bayesian analyses the 2GENE, 3GENE, and 4GENE
combined datasets were partitioned as described above. Mod-
eltest (Posada & Crandall, 1998) was used to estimate for each
dataset and each of the above partitions individually the number
of substitution types, to test for an implementation of a gamma
shape distribution (approximated with four categories) and to
test for a proportion of invariable sites. Three independent runs
with 30,000,000 generations, and four independent chains each
were started with MrBayes v.3.1.2 (Ronquist & Huelsenbeck,
2003) for each dataset, sampling every 500th tree. The tempera-
ture parameter for the (MC)3 chains of MrBayes was lowered
to 0.05 to ensure that a sufficient amount of state swapping oc-
curred across the four chains. The burn-in fraction of sampled
trees was estimated both by eye with ln-likelihood plots and
using AWTY (Nylander & al., 2008).
Only nodes that received posterior probabilities equal and
above 0.95 and ML-bootstrap support values equal or above
70% are interpreted as strongly supported.
RESULTS
DNA
sequences and test for topological incongruence.
A total of 201 new sequences were generated for this study,
including 43 nucITS, 49 nucLSU, 47 mitSSU, and 62 RPB1
sequences. The 1GENE-nucLSU dataset contained 353 taxa
with a total of 3242 characters, 1357 of which could be unam-
biguously aligned. The 1GENE-nucITS dataset had 731 taxa
an d 533 charac ters, with 366 al ignable positio ns. Th e 1GEN E -
mitSSU dataset contained 374 taxa with 2488 characters, 641
of which were unambiguous. The 1GENE-RPB1 dataset con-
tained 205 taxa, and 615 of 760 characters could be unambigu-
ously aligned. The test for topological incongruence (results
not shown) displayed no supported conf licts at or above the
generic level, and the single-gene datasets were thus combined
for further analysis.
Phylogenetic analyses. —
Analyses of three differ-
ent datasets were performed: all OTUs with at least two loci
(2GENE), at least three loci (3GENE), and a dataset only in-
cluding OTUs with all four genes available (4GENE). There
was no conflict (i.e., strongly supported conflicting topologies
with ≥75% bootstrap support) between the phylogenetic trees
obtained from these analyses and between ML and Bayes-
ian analyses of each of the datasets. The trees obtained in the
analyses on the 2GENE and 4GENE datasets are available as
Figs. S1–S2, whereas the 3GENE dataset tree, being the best
compromise between number of taxa and amount of missing
loci, is shown in Fig. 1.
The combined 3GENE dataset contained 323 OTUs (311
nucLSU, 315 nucITS, 307 mitSSU, 181 RPB1) and a total of
2970 characters, allowing for a maximum of one missing locus
per OTU. After excluding alignment positions with only unde-
termined character states (positions containing only Ns, gaps,
or missing data), the nucLSU remained with 1351 unambiguous
characters, and the mitSSU remained with 638 unambiguous
characters. The total number of included characters for nucITS
and R PB1 remained unchanged with 366 and 615 characters,
respectively.
The optimal ML tree estimated with RAxML (ln likeli-
hood = – 44,695.13) is show n in Fig. 1. Becau se infe rences from
RAxML, GARLI and the Bayesian analysis presented no con-
flict, the ML tree obtained using RAxML is shown with sup-
port from the other two methods of analysis included. The three
independent runs of MrBayes plateaued at different likelihood
levels, and after discarding the first 15,000,000 generations as
burn-in (50%), the last 30,000 trees of the best run were used
to calculate the posterior probabilities for internal branches.
Molecular phylogeny. —
A cartoon phylogeny that sum-
marises all generic relationships within Parmeliaceae that
are supported in at least one of the single-locus analyses is
presented in Fig. 2. The core group of parmelioid lichens as
circumscribed by Crespo & al. (2007) is monophyletic and
strongly supported in the 4GENE dataset, but does not receive
significant support in the 2GENE and 3GENE datasets. The
sister-group relationship of parmelioid lichens in Parmeliaceae
is not resolved with confidence, since the sister-group relation-
ship with Usnea lacks support in all datasets analyzed . Mono-
phyly of Parmeliaceae is strongly supported. Within parmelioid
lichens, several well-supported major clades are distinguished.
The Parmotrema clade includes the following monophyletic
genera: Parmotrema (with two individuals of Canoparme-
lia norstictica and one Parmelaria sp. nested within, and the
C. crozalsiana group as sister to the remaining Parmotrema
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Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
Parmotrema pseudoreticulatum
Parmotrema reticulatum 2
Parmotrema reticulatum 3
Parmotrema reticulatum 1
Parmotrema cetratum
Parmotrema hypoleucinum
Parmotrema perforatum
Parmotrema tinctorum 1
Parmotrema tinctorum 2
Parmotrema austrosinense
Parmotrema subthomsonii (syn=Parmelaria)
Parmotrema crinitum
Parmotrema perlatum
Parmotrema fistulatum
Parmotrema subcaperatum
Parmotrema norsticticatum 1 (syn=Canoparmelia norsticticata)
Parmotrema norsticticatum 2 (syn=Canoparmelia norsticticata)
Parmotrema pilosum
Parmotrema robustum
Parmotrema haitiense
Parmotrema subtinctorium
“Canoparmelia” carneopruinata
“Canoparmelia” crozalsiana
“Canoparmelia” inhaminensis
“Canoparmelia” schelpei
Flavoparmelia caperata2
Flavoparmelia caperata1
Flavoparmelia baltimorensis 2
Flavoparmelia baltimorensis 1
Flavoparmelia springtonensis
Flavoparmelia marchantii
Flavoparmelia haysomii
Flavoparmelia soredians
Flavoparmelia subambigua (syn=Pseudoparmelia subambigua)
Flavoparmelia citrinescens
Austroparmelina pseudorelicina
Austroparmelina labrosa
Austroparmelina pruinata
Austroparmelina endoleuca
Austroparmelina elixia
Austroparmelina conlabrosa
Punctelia subflava
Punctelia pseudocoralloidea
Punctelia rudecta2
Punctelia rudecta1
Punctelia subrudecta
Punctelia jeckeri
Punctelia perreticulata
Punctelia borreri
Punctelia reddenda
Punctelia hypoleucites
Punctelia sp.
Nesolechia oxyspora 1
Nesolechia oxyspora 2
Flavopunctelia flaventior 2
Flavopunctelia flaventior 1
Flavopunctelia soredica
Canoparmelia nairobiensis
Canoparmelia texana 2
Canoparmelia texana 1
Canoparmelia caroliniana 1
Canoparmelia caroliniana 2
Xanthoparmelia scotophylla
Xanthoparmelia lithophiloides
Xanthoparmelia subspodochroa
Xanthoparmelia norcapnodes
Xanthoparmelia lithophila
Xanthoparmelia crespoae 2
Xanthoparmelia crespoae 1
Xanthoparmelia murina
Xanthoparmelia digitiformis
Xanthoparmelia exornata
Xanthoparmelia perspersa 2
Xanthoparmelia perspersa 1
Xanthoparmelia scitula
Xanthoparmelia transvaalensis
Xanthoparmelia verrucigera
Xanthoparmelia subverrucigera
Xanthoparmelia isidiovagans
Xanthoparmelia vicentei
Xanthoparmelia conspersa 2
Xanthoparmelia atticoides
Xanthoparmelia sublaevis
Xanthoparmelia conspersa 1
Xanthoparmelia protomatrae
Xanthoparmelia stenophylla
Xanthoparmelia subdiffluens
Xanthoparmelia angustiphylla
Xanthoparmelia tinctina 1
Xanthoparmelia tinctina 2
Xanthoparmelia semiviridis
Xanthoparmelia subchalybaeizans 2
Xanthoparmelia subchalybaeizans 1
Xanthoparmelia ralla 2
Xanthoparmelia ralla 1
Xanthoparmelia chalybaeizans
Xanthoparmelia chlorea
Xanthoparmelia notata
Xanthoparmelia brachinaensis
Xanthoparmelia hottentotta
Xanthoparmelia hueana
Xanthoparmelia mougeotii 2
Xanthoparmelia mougeotii 1
Xanthoparmelia tegeta
bs)
bs)
bs+raxML bs)
Parmotrema-clade Xanthoparmelia-clade
Parmotrema pseudoreticulatum
Parmotrema reticulatum 2
Parmotrema reticulatum 3
Parmotrema reticulatum
1
1
Parmotrema cetratum
Parmotrema hypoleucinum
Parmotrema perforatum
Parmotrema tinctorum 1
Parmotrema tinctorum 2
Parmotrema austrosinense
Parmotrema subthomsonii (syn=Parmelaria)
Parmotrema crinitum
Parmotrema perlatum
Parmotrema fistulatum
Parmotrema subcaperatum
Parmotrema norsticticatum 1 (syn=Canoparmelia norsticticata)
Parmotrema norsticticatum 2 (syn=Canoparmelia norsticticata)
Parmotrema pilosum
Parmotrema robustum
Parmotrema haitiense
Parmotrema subtinctorium
“Canoparmelia” carneopruinata
“Canoparmelia” crozalsiana
“Canoparmelia” inhaminensis
“Canoparmelia” schelpei
Flavoparmelia caperata 2
Flavoparmelia caperata 1
Flavoparmelia baltimorensis 2
Flavoparmelia baltimorensis 1
Flavoparmelia springtonensis
Flavoparmelia marchantii
Flavoparmelia haysomii
Flavoparmelia soredians
Flavoparmelia subambigua (syn=Pseudoparmelia subambigua)
Flavoparmelia citrinescens
Austroparmelina pseudorelicina
Austroparmelina labrosa
Austroparmelina pruinata
Austroparmelina endoleuca
Austroparmelina elixia
Austroparmelina conlabrosa
Punctelia subflava
Punctelia pseudocoralloidea
Punctelia rudecta 2
Punctelia rudecta 1
Punctelia subrudecta
Punctelia jeckeri
Punctelia perreticulata
Punctelia borreri
Punctelia reddenda
Punctelia hypoleucites
Punctelia sp.
Nesolechia oxyspora 1
Nesolechia oxyspora 2
Flavopunctelia flaventior 2
Flavopunctelia flaventior 1
Flavopunctelia soredica
Canoparmelia nairobiensis
Canoparmelia texana 2
Canoparmelia texana 1
Canoparmelia caroliniana 1
Canoparmelia caroliniana 2
Xanthoparmelia scotophylla
Xanthoparmelia lithophiloides
Xanthoparmelia subspodochroa
Xanthoparmelia norcapnodes
Xanthoparmelia lithophila
Xanthoparmelia crespoae 2
Xanthoparmelia crespoae 1
Xanthoparmelia murina
Xanthoparmelia digitiformis
Xanthoparmelia exornata
Xanthoparmelia perspersa 2
Xanthoparmelia perspersa 1
Xanthoparmelia scitula
Xanthoparmelia transvaalensis
Xanthoparmelia verrucigera
Xanthoparmelia subverrucigera
Xanthoparmelia isidiovagans
Xanthoparmelia vicentei
Xanthoparmelia conspersa 2
Xanthoparmelia atticoides
Xanthoparmelia sublaevis
Xanthoparmelia conspersa 1
Xanthoparmelia protomatrae
Xanthoparmelia stenophylla
Xanthoparmelia subdiffluens
Xanthoparmelia angustiphylla
Xanthoparmelia tinctina 1
Xanthoparmelia tinctina 2
Xanthoparmelia semiviridis
Xanthoparmelia subchalybaeizans 2
Xanthoparmelia subchalybaeizans 1
Xanthoparmelia ralla 2
Xanthoparmelia ralla 1
Xanthoparmelia chalybaeizans
Xanthoparmelia chlorea
Xanthoparmelia notata
Xanthoparmelia brachinaensis
Xanthoparmelia hottentotta
Xanthoparmelia hueana
Xanthoparmelia mougeotii 2
Xanthoparmelia mougeotii 1
Xanthoparmelia tegeta
Supported with1 analysis
Supported with 2
Supported with 3
(pp+raxML bs+Garli
(pp, raxML bs,
( pp+raxML bs, Garli
Supported with1 analysis
Supported with 2 analyses
Supported with 3 analyses
(pp+raxML bs+Garli bs)
(pp, raxML bs,
(pp, raxML bs, Garli bs)
( pp+raxML bs, Garli( pp+raxML bs, Garli bs+raxML bs)
Parmotrema clade Xanthoparmelia clade
Fig. 1.
Phylogram obtained from
a ML analysis of the 3GENE
dataset (see text for details),
showing the phylogenetic rela-
tionships among Parmeliaceae.
Continued overleaf.
1740
TA XO N 59 (6) • December 2010: 1735–1753Crespo & al. • Generic classification of parmelioid lichens
Fig. 1.
Continued.
Xanthoparmelia azaniensis
Xanthoparmelia peltata
Xanthoparmelia ovealbornii
Xanthoparmelia pokornyi 1
Xanthoparmelia loxodes 2
Xanthoparmelia delisei
Xanthoparmelia aff glabrans
Xanthoparmelia pulloides
Xanthoparmelia pokornyi 2
Xanthoparmelia pulla
Xanthoparmelia loxodes 1
Xanthoparmelia subprolixa
Xanthoparmelia aff delisei
Xanthoparmelia subincerta
Xanthoparmelia glabrans
Xanthoparmelia saxeti
Cetrelia chicitae
Cetrelia cetrarioides
Cetrelia braunsiana
Cetrelia japonica
Cetrelia pseudolivetorum
Cetrelia olivetorum 2
Cetrelia olivetorum 1
Remototrachyna scytophylla
Remototrachyna ciliata
Remototrachyna flexilis 1
Remototrachyna koyaensis
Remototrachyna adducta
Remototrachyna infirma
Remototrachyna incognita
Remototrachyna crenata
Remototrachyna costaricensis
Bulbothrix sensibilis
Bulbothrix isidiza
Bulbothrix decurtata
Bulbothrix setschwanensis
Bulbothrix meizospora
Parmelinella wallichiana
Bulbothrix apophysata
Bulbothrix coronata
Bulbothrix goebelii
Parmelina pastillifera 2
Parmelina pastillifera 1
Parmelina tiliacea 1
Parmelina tiliacea 2
Parmelina coleae 1
Parmelina coleae 2
Parmelina coleae 3
Parmelina coleae 4
Parmelina carporrhizans 1
Parmelina carporrhizans 2
Parmelina carporrhizans 3
Parmelina quercina
Myelochroa aurulenta2
Myelochroa aurulenta1
Myelochroa irrugans
Myelochroa entotheiochroa
Myelochroa metarevoluta
Parmelinopsis subfatiscens
Parmelinopsis cryptochlora
Hypotrachyna exsecta
Parmelinopsis horrescens
Parmelinopsis minarum
Parmelinopsis neodamaziana
Parmelinopsis afrorevoluta
Hypotrachyna neodissecta
Hypotrachyna revoluta1
Hypotrachyna revoluta2
Hypotrachyna britannica
Hypotrachyna booralensis
Hypotrachyna polydactyla
Hypotrachyna osseoalba
Hypotrachyna immaculata
Hypotrachyna pseudosinuosa
“Hypotrachyna” physcioides
“ Hypotrachyna” imbricatula
“Hypotrachyna” laevigata
“Hypotrachyna” degelii
“Hypotrachyna” endochlora
“Hypotrachyna”taylorensis
“Hypotrachyna” rockii
“Hypotrachyna” caraccensis
“ Hypotrachyna” sinuosa
Everniastrum nepalense
Everniastrum rhizodendroideum
Everniastrum sorocheilum
Everniastrum vexans
Everniastrum cirrhatum
Cetrariastrum dubitans
Cetrariastrum andense
Everniastrum lipidiferum
Parmeliopsis hyperopta
Parmeliopsis ambigua
Nipponoparmelia laevior 2 (syn=Parmelia laevior)
Nipponoparmelia laevior 1 (syn=Parmelia laevior)
Nipponoparmelia ricasolioides 1 (syn=Parmelia ricasolioides )
“Parmelia” cunninghamii
“Parmelia” signifera
“Parmelia” tenuirima
“Parmelia” subtestacea
“Parmelia” crambidiocarpa
Relicina sydneyensis 1
Relicina subnigra
Relicina sydneyensis 2
Parmelia saxatilis 1
Parmelia saxatilis 2
Parmelia discordans
Parmelia serrana
Parmelia sulcata1
Parmelia sulcata2
Parmelia squarrosa
Cetrelia-
clade
Parmelina-clade
Hypotrachyna-clade
Parmeliopsis-clade
Parmelia-
clade
Xanthoparmelia azaniensis
Xanthoparmelia peltata
Xanthoparmelia ovealbornii
Xanthoparmelia pokornyi 1
Xanthoparmelia loxodes 2
Xanthoparmelia delisei
Xanthoparmelia aff glabrans
Xanthoparmelia pulloides
Xanthoparmelia pokornyi 2
Xanthoparmelia pulla
Xanthoparmelia loxodes 1
Xanthoparmelia subprolixa
Xanthoparmelia aff delisei
Xanthoparmelia subincerta
Xanthoparmelia glabrans
Xanthoparmelia saxeti
Cetrelia chicitae
Cetrelia cetrarioides
Cetrelia braunsiana
Cetrelia japonica
Cetrelia pseudolivetorum
Cetrelia olivetorum 2
Cetrelia olivetorum 1
Remototrachyna scytophylla
Remototrachyna ciliata
Remototrachyna flexilis 1
Remototrachyna koyaensis
Remototrachyna adducta
Remototrachyna infirma
Remototrachyna incognita
Remototrachyna crenata
Remototrachyna costaricensis
Bulbothrix sensibilis
Bulbothrix isidiza
Bulbothrix decurtata
Bulbothrix setschwanensis
Bulbothrix meizospora
Parmelinella wallichiana
Bulbothrix apophysata
Bulbothrix coronata
Bulbothrix goebelii
Parmelina pastillifera 2
Parmelina pastillifera 1
Parmelina tiliacea 1
Parmelina tiliacea 2
Parmelina coleae 1
Parmelina coleae 2
Parmelina coleae 3
Parmelina coleae 4
Parmelina carporrhizans 1
Parmelina carporrhizans 2
Parmelina carporrhizans 3
Parmelina quercina
Myelochroa aurulenta 2
Myelochroa aurulenta 1
Myelochroa irrugans
Myelochroa entotheiochroa
Myelochroa metarevoluta
Parmelinopsis subfatiscens
Parmelinopsis cryptochlora
Hypotrachyna exsecta
Parmelinopsis horrescens
Parmelinopsis minarum
Parmelinopsis neodamaziana
Parmelinopsis afrorevoluta
Hypotrachyna neodissecta
Hypotrachyna revoluta 1
Hypotrachyna revoluta 2
Hypotrachyna britannica
Hypotrachyna booralensis
Hypotrachyna polydactyla
Hypotrachyna osseoalba
Hypotrachyna immaculata
Hypotrachyna pseudosinuosa
“Hypotrachyna” physcioides
“ Hypotrachyna” imbricatula
“Hypotrachyna” laevigata
“Hypotrachyna” degelii
“Hypotrachyna” endochlora
“Hypotrachyna”taylorensis
“Hypotrachyna” rockii
“Hypotrachyna” caraccensis
“ Hypotrachyna” sinuosa
Everniastrum nepalense
Everniastrum rhizodendroideum
Everniastrum sorocheilum
Everniastrum vexans
Everniastrum cirrhatum
Cetrariastrum dubitans
Cetrariastrum andense
Everniastrum lipidiferum
Parmeliopsis hyperopta
Parmeliopsis ambigua
Nipponoparmelia laevior 2 (syn=Parmelia laevior)
Nipponoparmelia laevior 1 (syn=Parmelia laevior)
Nipponoparmelia ricasolioides 1 (syn=Parmelia ricasolioides)
“Parmelia” cunninghamii
“Parmelia” signifera
“Parmelia” tenuirima
“Parmelia” subtestacea
“Parmelia” crambidiocarpa
Relicina sydneyensis 1
Relicina subnigra
Relicina sydneyensis 2
Parmelia saxatilis 1
Parmelia saxatilis 2
Parmelia discordans
Parmelia serrana
Parmelia sulcata 1
Parmelia sulcata 2
Parmelia squarrosa
Cetrelia
clade
Parmelina cladeHypotrachyna clade
Parmeliopsis clade
Parmelia
clade
1741
Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
Fig. 1.
Continued.
0.1
Melanohalea aff exasperata1
Melanohalea aff exasperata2
Melanohalea aff exasperata3
Melanohalea exasperata1
Melanohalea elegantula 2
Melanohalea exasperata2
Melanohalea aff elegantula 1
Melanohalea aff elegantula 2
Melanohalea exasperatula 2
Melanohalea exasperatula 1
Melanohalea elegantula 1
Melanohalea subolivacea
Melanohalea septentrionalis
Melanohalea subelegantula
Melanohalea olivacea
Melanelixia subargentifera 2
Melanelixia subargentifera 1
Melanelixia glabra 2
Melanelixia villosella
Melanelixia albertana
Melanelixia glabra 1
Melanelixia subaurifera 2
Melanelixia subaurifera 1
Melanelixia fuliginosa 2
Melanelixia fuliginosa 1
Melanelixia pilliferella (syn=Melanelia pilliferella)
Melanelixia glabratuloides (syn=Melanelia glabratuloides)
Melanelixia calva (syn=Melanelia calva)
Melanelixia subglabra (syn=Melanelia subglabra)
Emodomelanelia masonii (syn=Parmelia masonii)
“Melanelia” disjuncta2
“Melanelia” sorediata
“Melanelia” disjuncta1
Pleurosticta acetabulum
“Melanelia” tominii
Evernia mesomorpha
Usnea antarctica 2
Usnea antarctica 1
Usnea sphacelata
Usnea trachycarpa
Usnea florida
Usnea longissima
Cetraria islandica 2
Cetraria islandica 1
Cetraria aculeata
Vulpicida pinastri 1
Vulpicida pinastri 2
Vulpicida juniperina
“Melanelia” sorediella
“Melanelia” commixta
Masonhalea richardsonii
Tuckermannopsis chlorophylla
Tuckermannopsis ciliaris
Cetreliopsis rhytidocarpa
Arctocetraria andrejevii
Flavocetraria nivalis 2
Flavocetraria nivalis 1
Dactylina arctica
Melanelia stygia 1
Melanelia stygia 2
Melanelia hepatizon
Platismatia glauca 1
Platismatia glauca 2
Platismatia norvegica
Omphalodium pisacomense 2
Omphalodium pisacomense 1
Imshaugia aleurites 1
Imshaugia aleurites 2
Pannoparmelia angustata
Protousnea magellanica
Letharia columbiana
Lethariella cashmeriana
Pseudevernia furfuracea 2
Pseudevernia furfuracea 1
Pseudevernia consocians
Hypogymnia vittata
Hypogymnia physodes
Arctoparmelia centrifuga
Brodoa oroarctica
Brodoa atrofusca
Brodoa intestiniformis
Evernia prunastri 2
Evernia prunastri 1
Menegazzia terebrata 1
Menegazzia terebrata2
Menegazzia myriotrema
Menegazzia confusa
Cetrariella delisei
Alectoria ochroleuca 1
Alectoria ochroleuca 2
Alectoria sarmentosa
Alectoria nigricans
Sulcaria sulcata
Sulcaria virens
Pseudephebe pubescens
Bryoria trichodes 2
Bryoria trichodes 1
Bryoria fuscescens
Bryoria capillaris
Bryoria fremontii
Allantoparmelia alpicola
Omphalora arizonica
Oropogon sperlingii
Psiloparmelia denotata
Everniopsis trulla
Cornicularia normoerica
Protoparmelia badia
Protoparmelia badia 1
Melanohalea-clade
OtherNon-parmelioid groups
Out group
0.1
Melanohalea aff exasperata 1
Melanohalea aff exasperata 2
Melanohalea aff exasperata 3
Melanohalea exasperata 1
Melanohalea elegantula 2
Melanohalea exasperata 2
Melanohalea aff elegantula 1
Melanohalea aff elegantula 2
Melanohalea exasperatula 2
Melanohalea exasperatula 1
Melanohalea elegantula 1
Melanohalea subolivacea
Melanohalea septentrionalis
Melanohalea subelegantula
Melanohalea olivacea
Melanelixia subargentifera 2
Melanelixia subargentifera 1
Melanelixia glabra 2
Melanelixia villosella
Melanelixia albertana
Melanelixia glabra 1
Melanelixia subaurifera 2
Melanelixia subaurifera 1
Melanelixia fuliginosa 2
Melanelixia fuliginosa 1
Melanelixia pilliferella (syn=Melanelia pilliferella)
Melanelixia glabratuloides (syn=Melanelia glabratuloides)
Melanelixia calva (syn=Melanelia calva)
Melanelixia subglabra (syn=Melanelia subglabra)
Emodomelanelia masonii (syn=Parmelia masonii)
“Melanelia” disjuncta 2
“Melanelia” sorediata
“Melanelia” disjuncta 1
Pleurosticta acetabulum
“Melanelia” tominii
Evernia mesomorpha
Usnea antarctica 2
Usnea antarctica 1
Usnea sphacelata
Usnea trachycarpa
Usnea florida
Usnea longissima
Cetraria islandica 2
Cetraria islandica 1
Cetraria aculeata
Vulpicida pinastri 1
Vulpicida pinastri 2
Vulpicida juniperina
“Melanelia” sorediella
“Melanelia” commixta
Masonhalea richardsonii
Tuckermannopsis chlorophylla
Tuckermannopsis ciliaris
Cetreliopsis rhytidocarpa
Arctocetraria andrejevii
Flavocetraria nivalis 2
Flavocetraria nivalis 1
Dactylina arctica
Melanelia stygia 1
Melanelia stygia 2
Melanelia hepatizon
Platismatia glauca 1
Platismatia glauca 2
Platismatia norvegica
Omphalodium pisacomense 2
Omphalodium pisacomense 1
Imshaugia aleurites 1
Imshaugia aleurites 2
Pannoparmelia angustata
Protousnea magellanica
Letharia columbiana
Lethariella cashmeriana
Pseudevernia furfuracea 2
Pseudevernia furfuracea 1
Pseudevernia consocians
Hypogymnia vittata
Hypogymnia physodes
Arctoparmelia centrifuga
Brodoa oroarctica
Brodoa atrofusca
Brodoa intestiniformis
Evernia prunastri 2
Evernia prunastri 1
Menegazzia terebrata 1
Menegazzia terebrata 2
Menegazzia myriotrema
Menegazzia confusa
Cetrariella delisei
Alectoria ochroleuca 1
Alectoria ochroleuca 2
Alectoria sarmentosa
Alectoria nigricans
Sulcaria sulcata
Sulcaria virens
Pseudephebe pubescens
Bryoria trichodes 2
Bryoria trichodes 1
Bryoria fuscescens
Bryoria capillaris
Bryoria fremontii
Allantoparmelia alpicola
Omphalora arizonica
Oropogon sperlingii
Psiloparmelia denotata
Everniopsis trulla
Cornicularia normoerica
Protoparmelia badia
Protoparmelia badia 1
Melanohalea-cladeOtherNon-parmelioid groups
Outgroup
2
1742
TA XO N 59 (6) • December 2010: 1735–1753Crespo & al. • Generic classification of parmelioid lichens
spp.), Flavoparmelia (with one Pseudoparmelia sp. nested
with i n), Austroparmelina, Punctelia, Nesolechia, Flavopunc-
telia, and Canoparmelia s.str. The relationships among these
lineages are strongly supported. The Xanthoparmelia clade
is sister to the Parmotrema clade and this relationship is only
supported in the Bayesian analysis. The former clade consists
of a monophyletic genus Xanthoparmelia. The phylogenetic
placement of the strongly supported, monophyletic genus Ce-
trelia is not recovered with confidence.
The Parmelina clade is strongly supported as monophyletic
including the monophyletic genera Myelochroa and Parmelina,
and in addition includes the monophyletic genus Remototra-
chyna and a paraphyletic Bulbothrix. In the 2GENE tree (Fig.
S1), both specimens of Hypotrachyna radiculata compose a
strongly supported lineage that is nested within Myelochroa. T h e
strongly supported monophyletic Hypotrachyna clade includes
the polyphyletic genera Everniastrum, Hypotrachyna, Parmeli-
nopsis, and a monophyletic Cetrariastrum. In the 2GENE tree
(Fig. S1), Cetrariastrum is nested within Everniastrum, but th i s
relationship lacks support. The genera Parmeliopsis and the
new genus Nipponoparmelia each form monophyletic groups
with uncertain relationships. Relicina is strongly supported as
monophyletic (including Relicinopsis in the 2GENE analysis,
Fig. S1). The relationships of Relicina s.l., however, remain un-
certain. Parmelia is polyphyletic, with one clade, segregated as
Nipponoparmelia below with uncertain relationships, a clade
of southern Hemisphere species (Parmelia spp. in Fig. 1) that
is sister to Relicina, but without support, Parmelia masonii
Fig. 2.
Cartoon tree summa-
rizing our current k nowledge
of phylogenetic relationships
within Parmeliaceae. Only
relationships that received sig-
nificant suppor t in at least one
of the analyses part of this study
are shown. Numbers of species
in each clade are in parentheses.
Parmotrema (350)
Flavoparmelia (35)
Austroparmelina (7)
Punctelia (34)
Nesolechia (4)
Flavopunctelia (7)
Canoparmelia s.str. (40)
Xanthoparmelia (819)
Cetrelia (18)
Parmelinopsis (25)
Hypotrachyna 1” (3)
Hypotrachyna s.str. (156)
Hypotrachyna 2” (15)
Everniastrum (40)
Cetrariastrum (4)
Remototrachyna (15)
Bulbothrix and Parmelinella (19)
Bulbothrix s.str. (15)
Myelochroa (28)
Parmelina (5)
Melanelixia (15)
Melanohalea (19)
Emodomelanelia (1)
Melanelia 1” and Pleurosticta (8)
Parmelia 1” (13)
Nipponoparmelia (4)
Parmelia s.str. (30)
Parmeliopsis (6)
Relicina and Relicinopsis (59)
Tuckermannopsis (11)
Arctocetraria (2)
Cetreliopsis (8)
Flavocetraria (2)
Cetraria (30)
Vulpicida (6)
Melanelia 2” (2)
Masonhalea (1)
Dactylina (9)
Melanelia s.str. (2)
Sulcaria (4)
Pseudephebe (3)
Alectoria (8)
Psiloparmelia (12)
Everniopsis (1)
Pannoparmelia (5)
Protousnea (8)
Menegazzia (60)
Cetrariella (2)
Letharia (5)
Lethariella (11)
Usnea (ca. 500)
Allantoparmelia (3)
Arctoparmelia (5)
Asahinea (4)
Brodoa (3)
Bryoria (75)
Cornicularia (1)
Evernia (5)
Hypogymnia (50)
Imshaugia (2)
Omphalodium (1)
Omphalora (1)
Oropogon (40)
Platismatia (10)
Pseudevernia (4)
Protoparmelia (20)
parmelioid
clade
Canoparmelia 1” (4)
1743
Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
as sister to Melanelixia + Melanoh alea, and Parmelia s.s tr.
(Parmelia spp. in Fig. 1); Parmelia s.str. is strongly supported
as monophyletic, but lacking support regarding intergeneric
relationships. The Melanelixia and Melanohalea clades form
one well supported clade in the 4GENE analysis (Fig. S2), but
do not receive significant support in the 2GENE or 3GENE
analyses (Fig. S1 and Fig. 1, resp.). Melanohalea is monophyletic
and Melanelixia as well, with a strongly supported sister-group
relationship to four species from the southern Hemisphere (pre-
viously placed in Melanelia) that are transferred to Melanelixia
below. Three other Melanelia spp. (M. disjuncta, M. sorediata,
M. tominii) cluster in one monophyletic group with Pleurosticta
acetabulum.
The phylogeny of non-parmelioid Parmeliaceae is beyond
the focus of this paper and will not be discussed in detail here.
The well-supported relationships agree mostly with those
discussed in Crespo & al. (2007), including strongly sup-
ported monophyly of alectorioid (Alectoria incl. Gowardia,
Pseudephebe, Sulcaria), cetrarioid (Arctocetraria, Cetraria,
Cetreliopsis, Dactylina, Flavocetraria, Melanelia, Tucker-
mannopsis, Vulpicida), letharioid (Letharia, Lethariella), and
psiloparmelioid lichens (Everniopsis, Psiloparmelia). Rela-
tionships among these groups and other monophyletic genera
(e.g., Bryoria, Platismatia) remain largely unresolved. A more
thorough taxon and gene sampling is needed to further assess
phylogenetic relationships of these groups in Parmeliaceae.
A number of species in parmelioid lichens do not form
monophyletic groups (e.g., Canoparmelia texana, Hypotrachyna
revoluta, Melanelia disjuncta, Melanohalea exasperata, Par-
melina tiliacea, Parmotrema reticulatum, Punctelia rudecta,
Xanthoparmelia pulla; Fig. S1), ind icating that addit iona l stud-
ies are necessary to clarify their current delimitations, which
are largely based on morphological and chemical characters.
TAXONOMY
Although there is a growing body of studies focused on
certain groups of parmelioid lichens, ours is the first study
addressing generic classification of parmelioid lichens as a
whole using molecular data. Our analyses confirm previous
studies that the generic classification is in need of further revi-
sion, with several genera being para- or polyphyletic. Here we
present a new generic classification based on our phylogenetic
studies and morphological and chemical evidence, listed al-
phabetically wit hin major clade s as indicated in Figs. 1 and 3.
Each of the clades and genera are briefly characterized mor-
phologically (Fig. 4), anatomically, and chemically. Taxonomic
changes are only proposed for well-supported clades. A new
genus, Emodomelanelia is described here, Nipponoparmelia
is elevated to generic rank, and an additional 15 new com-
binations are proposed. The genus Parmelaria is reduced to
synonymy with Parmotrema. We identify several groups for
which additional taxon sampling and/or generation of mo-
lecular data are necessary for unequivocal resolution of their
phylogenetic placement. Data on conidia were studied for the
included species.
1. Parmotrema clade
Th is cla de includes spe cies that contain a not wel l charac-
terized but diagnostic cell wall polysaccharide (isolichenan).
Most species have a pored epicortex, some have pseudocyphel-
lae, and they contain either atranorin or usnic acid as a cortical
pigment (Fig. 4A–D). The center of diversity is in the Southern
Hemisphere, with numerous tropical and subtropical species,
some of which extend into temperate regions (Blanco & al.,
2005, 2006).
Austroparmelina A. Cresp o, Divak a r & Elix in Syst. Biodiver s.
8: 216. 2010 – Type: A. pseudorelicina (Jatta) A. Crespo
& al. in Syst. Biodivers. 8: 217. 2010 (Parmelia pseudo-
relicina Jatta in Boll. Soc. Bot. Ital., 1910: 254. 1911).
Fig. 3.
Nine major groups withi n the parm elioid clade of Pa r meliacea e
sharing morphological and chemical characters. This is a cartoon
tree summarizing our current knowledge of phylogenetic relation-
ships based on nucITS, mitSSU, nucLSU, and RPB1 single-locus and
combined datasets discussed in the text. Naming and numbering of
the clades follows descriptions in the text. The size of the triangles
and nu mber behind the triangles indicate the number of species cur-
rently included in each of the clades. Branch lengths in this tree are
uninformative. *The Parmelia clade is not supported in molecular
analyses, but due to shared morphological and chemical characteres
we are treating the included taxa together in the text.
1. Parmotrema clade
Canoparmelia 1”
Flavoparmelia
Austroparmelina
Punctelia
Nesolechia
Flavopunctelia
Canoparmelia s.str.
2. Xanthoparmelia clade
3. Cetrelia clade
Parmelinopsis
Hypothrachyna 2”
Hypotrachyna 1”
5. Hypotrachyna clade
Everniastrum
Remototrachyna
Bulbothrix and Parmelinella
Bulbothrix s.str.
Myelochroa
4. Parmelina clade
Melanelixia
Melanohalea
Emodomelanelia
Melanelia 1” and Pleurosticta
Parmelia 1”
Parmeliopsis
Nipponoparmelia
Parmelia s.str.
Parmotrema
Xanthoparmelia
Cetrelia
Parmelina
Hypotrachyna s.str.
Cetrariastrum
6. Parmeliopsis clade
7. Nipponoparmelia clade
8. Parmelia clade*
9. Melanohalea clade
819
481
243
82
18
6
102
43
4
Relicina and Relicinopsis
parmelioid
clade
174 4
TA XO N 59 (6) • December 2010: 1735–1753Crespo & al. • Generic classification of parmelioid lichens
Fig. 4.
Selected species representing clades and genera in the parmelioid Parmeliaceae.
A–D,
Parmotrema clad e:
A,
Canoparmelia texana;
B,
Fla-
voparmelia flaventior;
C,
Parmotrema tinctorum;
D,
Punctelia subrudecta.
E,
Xanthoparmelia clade: X. exornata.
F,
Cetrelia clade: C. braun-
siana.
GI,
Parmelina clade:
G,
Bulbothrix suffixa;
H,
Myelochroa irrugans;
I,
Parmelina tiliacea.
J–L,
Hypotrachyna cla de:
J,
Everniastrum
cirrhatum;
K,
Hypotrachyna imbricatula;
L,
Parmelinopsis horrescens.
M,
Parmelia cla de: P. sulcata.
NO,
Melanohalea clade:
N,
Melanohalea
exasperata;
O.
Pleurosticta acetabulum.
1745
Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
Diagnostic characters. – Lobes subirregular; pored epi-
cortex present; isolichenan; conidia cylindrical.
Notes. – The genus Austroparmelina was recently de-
sc r ibed (Cresp o & al., 2010) for spe cie s prev iou sly pla ced in th e
polyphyletic genera Canoparmelia and Parmelina. This genus
is sister to a clade comprising F lavoparmelia + Parmot rema.
It differs from Parmotrema in having adnate thalli, narrow
lobes, rhizines on the lower surface extending to the margins
and cylindrical conidia; and from Flavoparmelia in having a
grey upper cortex (containing atranorin). The monophyly of
this genus and its relationships are well-supported. Crespo & al.
(2007) showed that “Canoparmelia pruinata was not related
to Canoparmelia s.str. Broadening taxon sampling to other
species of Canoparmelia revealed (Fig. 1) that several species
occurring in the Southern Hemisphere composed a novel clade
in need of taxonomic recognition.
Canoparmelia Eli x & Hale in Mycot a xon 27: 277. 1986 – Type:
C. texana (Tuck.) Elix & Hale in Mycotaxon 27: 279. 1986
(Parmelia texana Tuck., in Amer. J. Sci. Arts, Ser. 2, 25:
424. 1858).
Diagnostic characters. – Lobes subirregular (Fig. 4A);
pored epicortex present; isolichenan; conidia bifusiform.
Notes. – In its restricted circumscription, this genus in-
cludes species wit h broad and la rge ascospores, la ck ing dep-
sidones and having a maculate upper surface. The genus in its
restricted sense is a strongly supported monophyletic group
whose common ancestry with the remaining genera within
the Parmotrema clade is also strongly supported (Fig. 1).
Molecular data suggest that Canoparmelia as originally cir-
cumscr ibed (Elix & al., 1986) is highly poly phyletic. Blanco
and colleagues (Blanco & al., 2004b, 2005) showed that some
Canoparmelia species clustered close to Parmotrema, and
subsequently, Crespo & al. (2007) demonstrated that other
Canoparmelia species were sister to Flavoparmelia and Par-
motrema. These species were subsequently placed in the new
genus Austroparmelina (Crespo & al., 2010). Here, we have
found an additional species, Canoparmelia norsticticata,
nested within Parmotrema (Fig. 1). This species is trans-
ferred to Parmotrema below, but the C. crozalsiana group
that composes the sister lineage to Parmotrema requires ad-
ditional study.
Flavoparmelia Hale in Mycotaxon 25: 604. 1986 – Type:
F. caperata (L.) Hale in Mycotaxon 25: 604. 1986 (Lichen
caperatus L., Sp. Pl. 2: 1147. 1753).
Diagnostic characters. – Broad lobes (Fig. 4B); pored epi-
cortex present; isolichenan; conidia bifusiform; cortex with
usnic acid.
Notes. – This genus was originally described as a segre-
gate of Pseudoparmelia to accommodate species with broad
lobes, containing usnic acid, isolichenan in cell walls, large
ascospores and marginally erhizinate lobes (Hale, 1986b; Elix,
1993). The phylogeny of Flavoparmelia is currently under
study (Blanco pers. comm.). The genus is sister to Parmotrema
from which it differs in having bifusiform conidia and always
containing usnic acid. Our analyses suggest the placement of
Pseudoparmelia subambigua within Flavoparmelia and con-
sequently it is here transferred to this genus.
Flavoparmelia citrinescens (Gyelnik) O. Blanco, A. Crespo
& Elix, comb. nov. [MB 516787] Parmelia citrinescens
Gyelnik in Ann. Mycol. 36: 271. 1938.
Flavoparmelia subambigua (Hale) O. Blanco, A. Crespo &
Elix, comb. nov. [MB 516752] ≡ Pseudoparmelia subam-
bigua Hale in Smithsonian Contr. Bot. 31: 50. 1976.
Flavopunctelia (Krog) Hale in Mycotaxon 20: 682. 1984
Ty p e : F. flaventior (Stirt.) Hale in Mycotaxon 20: 682.
1984 (Parmelia flaventior Stirt. in Trans. Glasgow Soc.
Field- Naturalists 5: 212. 1877).
Diagnostic characters. – Lobes subirregular; non-pored
epicortex, with punctiform pseudocyphellae; isolichenan; co-
nidia bifusiform; containing usnic acid.
Notes. – This genu s was or igina lly descr ibed as a su bgenus
of Punctelia (Krog, 1982), but was later raised to generic level
(Hale, 1984a) based on differences in conidial morphology.
Molecular studies confirm the distinction of these two groups
with roundish pseudocyphellae at generic level. This small
genus (7 species) occurs in temperate and tropical regions on
all continents except Australia.
Nesolechia A. Ma s s a l ., Misc. Lichenol.: 43. 1856 Typ e: N. oxy -
spora (Tul.) A. Massal., Misc.Lichenol.: 43. 1856 (Abro-
thallus oxysporus Tul. in Ann. Sci. Nat., Bot., sér. 3, 17:
116. 1852).
Diagnostic characters. – Lichenicolous fungus; gall form-
ing; thallus endokapylic; apothecia with entire margin; conidia
bacilliform.
Notes. – The genus Nesolechia was treat ed as a sy n ony m of
Phacopsis Tul. by Triebel & Rambold (1988) based on the ab-
sence of great anatomical differences between both genera. This
was not accepted by some authors and Alstrup & Haswksworth
(1990) offered several characters in which both genera differ.
Subse que ntly, Die derich (2003) supp orted congener i t y base d on
similarities of epihymenial and hypothecial pigments. The mo-
lecular study of species of Phacopsis a nd Nesolechia by Peršoh
& Rambold (2002) revealed their placement in Parmeliaceae for
the first time, later supported by Crespo & al. (2007). However
results in Peršoh & Rambold (2002) revealed the polyphyly
of the genus Phacopsis. Thus, until further research is made
in this group we propose to keep the name Nesolechia. In our
analysis specimens of Nesolechia represent the sister group to
the genus Punctelia; this relationship is well-supported in all
the trees generated.
Parmotrema A. Massal. in Atti Reale Veneto Sci. Lett. Arti,
se r. 3, 5: 248. 1860 – Type: P. perforatum (Wu l fen) A. Mas-
sal. in Atti Reale Veneto Sci. Lett. Arti, ser. 3, 5: 248. 1860
(Lichen perforatus Wulfen in Jacquin, Collectanea 1: 116.
178 7 [‘17 86’] ).
= Canomaculina Elix & Hale in Mycotaxon 29: 239. 1987
Ty p e : C. pilosa (Stizenb.) Elix & Hale in Mycotaxon 29:
1746
TA XO N 59 (6) • December 2010: 1735–1753Crespo & al. • Generic classification of parmelioid lichens
240. 1987 (Parmelia pilosa Stizenb. in Ber. Thätigk. St.
Gallischen Naturwiss. Ges., 1888–89: 165. 1890).
= Concamerella W.L. Culb. & C.F. Culb. in Bryologist 84:
307. 1981 – Type: C. pachyderma (Hue) W.L. Culb. &
C.F. Culb. in Bryologist 84: 308. 1981 (Parmelia pachy-
derma Hue in Nouv. Arch. Mus. Hist. Nat., ser. 4, 1: 137.
189 9).
= Parmelaria D.D. Awas t h i in J. Hatto r i Bot . Lab. 63: 368 . 1987
– Type: P. thomsonii (Stirt.) D.D. Awasthi in J. Hattori Bot.
Lab. 63: 368. 1987 (Platysma thomsonii Stirt. in Proc. Roy.
Phil. Soc. Glasgow 11: 321. 1879), sy n. nov.
= Rimelia Hale & A. Fletcher in Bryologist 93: 23. 1990
Ty p e : R. cetrata (Ach.) Hale & A. Fletcher in Bryologist
93: 26. 1990 (Parmelia cetrata Ach., Syn. Meth. Lich.: 198.
1814).
= Rimeliella Kurok. in Ann. Tsukuba Bot. Gard. 10: 1. 1991 –
Ty p e : R. subcaperata (Kremp.) Kurok. in Ann. Tsukuba
Bot. Gard. 10: 7. 1991 (Parmelia subcaperata Kremp. in
Vidensk. Meddel. Dansk Naturhist. Foren. Kjøbenhavn,
ser. 3, 1873: 10. 1873).
Diagnostic characters. – B roa d lob es (Fig. 4C); por ed epi -
cortex present; intermediate-type lichenan between Cetraria-
type and Xanthoparmelia-type lichenan; conidia cylindrical.
Notes. – The genus as now circumscribed includes ca. 350
species that have their center of distribution in tropical regions
of the world, especially in the Pacific Islands and South Amer-
ica (Blanco & al., 2005). The genus is sister to Flavoparmelia.
Our analysis confirms the placement of Parmelaria within
Parmotrema (the type of Parmelaria, P. thomsonii, clustered
within Parmotrema in a single-gene analysis, data not shown)
and consequently the two Parmelaria spp. and the species pre-
viously classified in Canoparmelia sensu lato, but which cluster
in Parmotrema are transferred to Parmotrema.
Parmotrema norsticticatum (G.N. Stevens) A. Crespo, Di-
vakar & Elix, comb. nov. [MB 516753] ≡ Parmelia nor-
sticticata G.N. Stevens in Austral. J. Bot. 27: 881. 1980. ≡
Canoparmelia norsticticata (G.N. Stevens) Elix & Hale in
Mycotaxon 27: 278. 1986.
Parmotrema subthomsonii (D.D. Awa sthi) A. Cr espo, Div akar
& Elix, comb. nov. [MB 516754] ≡ Parmelaria subthom-
sonii D.D. Awasthi in J. Hattori Bot. Lab. 63: 370. 1987.
Parmotrema thomsonii (Stirt.) A. Crespo, Divakar & Elix,
comb. nov. [MB 516755] ≡ Platysma thomsonii Stirt. in
Proc. Roy. Phil. Soc. Glasgow 11: 321. 1879 ≡ Parmelaria
thomsonii (Stirt.) D.D. Awasthi in J. Hattori Bot. Lab. 63:
36 8 . 19 8 7.
Punctelia Krog in Nord. J. Bot. 2: 290. 1982Type: P. borreri
(Sm.) Krog in Nord. J. Bot. 2: 291. 1982 (Lichen borreri
Sm. in Engl. Bot. 25: tab. 1780. 1807).
Diagnostic characters. – Lobes subirregular; non-pored
epicortex, punctiform pseudocyphellae present (Fig. 4D); isoli-
chenan; conidia unciform or cylindrical; containing atranorin,
lacking usnic acid.
Notes. – This genus of ca. 45 species is cosmopolitan with
highes t diversity in the Neot ropics and Afric a. The most si m ilar
genus is Flavopunctelia, which differs in conidial morphology
and the presence of usnic acid (Krog, 1982; Hale, 1984a). The
genus is well-supported as monophyletic sister to Nesolechia.
2. Xanthoparmelia clade
This clade includes only the genus Xanthoparmelia, after
Karoowia was recently included in Xanthoparmelia (Amo &
al., 2010b). The clade includes spec ie s that have cel l wall poly-
saccharides with Xanthoparmelia-type lichenan. Most species
occur in the Southern Hemisphere in arid or semiarid subtropi-
cal areas, with some extending into temperate regions. The spe-
cies in this clade lack true pseudocyphellae, have a pored epi-
cortex (Fig. 4E), and show a considerable variation in cortical
chemistry, including species containing usnic acid, atranorin
or lacking cortical phenols (Blanco & al., 2004b; 2006).
Xanthoparmelia (Vain.) Hale in Phytologia 28: 485. 1974 –
Ty p e : X. conspersa (Ehrh. ex Ach.) Hale in Phytologia 28:
485. 1974 (Lichen conspersus Ehrh. ex Ach., Lichenogr.
Suec. Prodr.: 118. 1798).
= Almbornia Essl. in Nord. J. Bot. 1: 125. 1981 – Type: A. caf-
ferensis Essl. in Nord. J. Bot. 1: 125. 1981.
= Chondropsis Nyl. ex Cromb. in J. Linn. Soc., Bot. 17: 397.
1879 – Type: C. semiviridis (F. Muell. ex Nyl.) Nyl. ex
Cromb. in J. Linn. Soc., Bot. 17: 397. 1879 (Parmeliopsis
semiviridis F. Muell. ex Nyl., Syn. Meth . Lich. 2: 57. 1869).
= Karoowia Hale in Mycotaxon 35: 182. 1989 – Type: K. ad-
haerens (Nyl.) Hale in Mycot axon 35: 182. 1989 (Parmelia
adhaerens Nyl. in J. Bot. 14: 19. 1876).
= Namakwa Hale in Mycotaxon 32: 169. 1988 – Type: N. exor-
nata (Zahlbr.) Hale in Mycotaxon 32: 169. 1988 (Parmelia
conturbata var. exornata Zahlbr. in Ann. Cryptog. Exot.
5: 251. 1932).
= Neofuscelia Essl. in Mycotaxon 7: 49. 1978 – Type: N. pulla
(Ach.) Essl. in Mycotaxon 7: 52. 1978 (Parmelia pulla Ach.,
Syn. Meth. Lich.: 206. 1814).
= Omphalodiella Henssen in Lichenologist 23: 334. 1991 –
Ty p e : O. patagonica Henssen in Lichenologist 23: 335.
1991.
= Paraparmelia Elix & J. Johnst. in Mycotaxon 27: 279. 1986
– Type: P. scotophylla (Ku rok .) Eli x & J. Joh n st. in Myc o -
ta xon 27: 281. 1986 (Parmelia scotophylla Ku r ok. in Cont r.
U.S. Natl. Herb. 36: 185. 1964).
= Placoparmelia Henssen in Lichenologist 24: 134. 1992 – Type:
P. patagonica Henssen in Lichenologist 24: 134. 1992.
= Xanthomaculina Hale in Lichenologist 17: 262. 1985 – Type:
X. hottentotta (Ach.) Hale in Lichenologist 17: 264. 1985
(Lichen hottentottus Ach., Lichenogr. Suec. Prodr.: 155.
179 8).
Diagnostic characters. – Pored epicortex present; Xan-
thoparmelia-type lichenan; conidia bifusiform or cylindrical;
ascospores arachiform
Notes. – The genus Xanthoparmelia was the subject of
several recent phylogenetic studies, resulting in a merging of a
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Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
number of previously recognized genera within it (Bla nco & al .,
2004b; Thell & al., 2006; Amo & al., 2010a,b); the most recent
being Karoowia, Omphalodiella and Placoparmelia (Amo &
al., 2010a,b). The clade is well-supported as monophyletic, but
the absence of distinct morphological traits associated with
well-supported monophyletic groups within the Xanthopar-
melia clade prevents the recognition of smaller genera within
this large genus. Morphological variation within this clade is
likely to be driven by environmental factors and were over-
emphasized in previous classifications (Lumbsch & al., 2008).
3. Cetrelia clade
This clade consists only of the genus Cetrelia, which was
traditionally regarded as cetrarioid based on the presence of
marginal apothecia, but is now considered to belong to parmeli-
oid lichens based on inferences from molecular data (Crespo
& al., 2007). The genus has broadly lobed thalli and was pre-
viously regarded as a “parmelioid Cetraria (Culberson &
Culberson, 1968). Furthermore, Cetrelia has isolichenan as
cell wall polysaccharide (Elix, 1993), which occurs in several
groups of parmelioid genera, but is absent in the cetrarioid
group (Crespo & al., 2007).
Cetrelia W.L. Culb. & C.F. Culb. in Contr. U.S. Natl. Herb. 34:
490. 1968 Ty pe: C. cetrarioides (Delise) W.L. Culb. &
C.F. Culb. in Contr. U.S. Natl. Herb. 34: 498. 1968 (Par-
melia perlata var. cetrarioides Delise in Duby, Bot. Gall.
Pars Secunda: 601. 1830).
Diagnostic characters. – Broad lobes (Fig. 4F); non-pored
epicortex, punctiform pseudocyphellae present; isolichenan;
conidia bifusiform; apothecia marginal.
4. Parmelina clade
The Parmelina clade is enlarged from its previous concept
(Blanco & al., 2006) to include Bulbothrix, Parmelinella and
Remototrachyna in agreement with Divakar & al. (2010) as
well as Myelochroa and Parmelina. The latter three genera
were previously placed in the Hypotrachyna clade, but the re-
lationships of these genera within the Hypotrachyna clade, in
a restricted sense, lacked support. Species in the Parmelina
clade have isolichenan in the cell walls, a pored epicortex, lack
pseud ocyph ell ae, an d con t ain at ra norin or usnic acid as cortical
compounds (Fig. 4G–I).
Bulbothrix Hale in Phytologia 28: 479. 1974 – Type: B. semi-
lunata (Ly nge) Hale in Phy t ologia 28: 479. 1974 (Parmelia
semilunata Lynge in Ark. Bot. 13: 23. 1914).
Diagnostic characters. – Lobes subirregular (Fig. 4G);
conidia cylindrical or bifusiform; bulbate cilia present.
Notes. – The circu mscr i ption of this genu s rema ins unc er-
ta i n. In curre nt phylog enie s, the genu s is par aphyletic. We have
so far not been able to get sequences of the species that includes
the type of the name and our taxon sampling is still poor. Ad-
ditional data are required to address the issue of monophyly
and circumscription of Bulbothrix.
Myelochroa (Asahina) Elix & Ha le in Mycotaxon 29: 24 0. 1987
– Type: M. aurulenta (Tuck.) Elix & Hale in Mycotaxon
29: 240. 1987 (Parmelia aurulenta Tuck. in Amer. J. Sci.
Arts, ser. 2, 25: 424. 1858).
Diagnostic characters. – Lobes subirregular (Fig. 4H);
conidia cylindrical or bifusiform; yellow-orange medulla
(secalonic acid derivatives).
Notes. – This relatively small genus (ca. 30 species) has its
center of distribution in eastern Asia and is characterized by the
presence of yellow-orange pigments (secalonic acid derivatives)
in the medulla and simple to squarrosely branched rhizines. It
is morphologically similar to Parmelina, which is also sister
to it, but the latter differs in having a white medulla and lack-
ing hopane triterpenes. Interestingly, these two clades have
a largely vicariant distribution: while Myelochroa is chiefly
distributed in eastern Asia, Parmelina is largely confined to
wi nter-r ain area s in the west of Europe and Nor th Am erica and
adjacent regions. The status of the two genera merits further
study. Results from Divakar & al. (2006) show the phylogenetic
placement of Hypotrachyna radiculata within Myelochroa.
Consequently, it is here transferred to this genus.
Myelochroa radiculata (Kurok.) Divakar & A. Crespo, comb.
nov. [MB 516756] ≡ Parmelia radiculata Kurok., Studies
Crypt. Papua New Guinea: 139. 1979 Parmelina radicu-
lata (Ku r ok.) St rei m a n n in Biblioth. Lichen ol. 22: 92. 1986
Parmelinopsis radiculata (Ku rok .) Eli x & Hale in Myco-
taxon 29: 243. 1987 ≡ Hypotrachyna radiculata ( K u r o k .)
Elix in Austral. Lichenol. 48: 35. 2001.
Parmelina Hale in Phytologia 28: 481. 1974 – Type: P. tiliacea
(Hoffm.) Hale in Phytologia 28: 481. 1974 (Lichen tiliaceus
Hoffm., Enum. Lich.: 96. 1784).
Diagnostic characters. – Lobes subirregular (Fig. 4I); co-
nidia cylindrical; medulla white; upper part of inner excipulum
carbonized.
Notes. – When originally described, the genus Parmelina
(Hale, 1974) included a number of unrelated elements that were
subsequently placed elsewhere (Elix & Hale, 1987; Crespo &
al., 2010). In its restricted sense, the genus is confined to the
Northern Hemisphere with a center of distribution in western
North America and Europe. In apothecial sections a thin car-
bonized layer is seen in the upper part of the inner excipulum,
corresponding to an amphithecial ring seen in a superficial
view of the ascomata. The closest relative, Myelochroa, is
mainly distinguished from it based on chemical characters.
Parmelinella Elix & Hale in Mycotaxon 29: 241. 1987 – Type:
P. wallichiana (Taylor) Elix & Ha le in Myc otaxon 29: 242 .
1987 (Parmelia wallichiana Taylor in London J. Bot. 6:
176. 1847).
Diagnostic characters. – Lobes subirregular; conidia cy-
lindrical or bifusiform; bulbate cilia absent; yellow-grey upper
cortex (secalonic acid derivatives).
Notes. – Parmelinella is nested within a clade of Bulbothrix
and its generic status is in need of revision. A study address-
ing the generic concept in the Bulbothrix/Parmelinella group
1748
TA XO N 59 (6) • December 2010: 1735–1753Crespo & al. • Generic classification of parmelioid lichens
requires more thorough taxon sampling. Under the current
generic circumscription, this small genus of three species is
distinguished from Bulbothrix mainly by the absence of bulbate
cilia and the presence of secalonic acid derivatives, characters
that are not supported as taxonomically important in molecular
phylogenies of parmelioid lichens (Divakar & al., 2006).
Remototrachyna Divakar & A. Crespo in Amer. J. Bot. 97: 584.
2010 – Type: R. flexilis (Kurok.) Divakar & A. Crespo in
Amer. J. Bot. 97: 586. 2010 (Parmelia f lexilis Kurok. in
Hara, Fl. Eastern Himalaya: 607. 1966).
Diagnostic characters. – Lobes broad; conidia bifusiform;
outer exciple with very thick cell walls.
Notes. – This recently described genus (Divakar & al.,
2010) was previously included in Hypotrachyna, but is not
closely related to that genus, from which it differs in lobe mor-
phology, rhizine length, hymenium height, exciple structure,
and ascospore size. Remototrachyna is distinguished from
Bulbothrix by having broader lobes, lacking bulbate cilia, a
higher hymenium, and larger ascospores. Remototrachyna has
its center of distribution in Southeast Asia.
5. Hypotrachyna clade
This clade includes the genera Cetrariastrum, Evernias-
trum, Hypotrachyna, and Parmelinopsis. All have isolichenan
as cell wall polysaccharide. They are currently poorly known
and have their center of species diversity in the tropical and
subtropical regions of both Hemispheres. All taxa in this clade
have a pored epicortex and lack pseudocyphellae (Fig. 4J–L).
They may contain atranorin, usnic acid or lichexanthone as
cortical substances. Some of the genera in this clade are not
monophyletic. However, since the backbone of the phylogeny
within the group is lacking support, we refrain from drawing
nomenclatural conclusions before additional data become avail-
able.
Cetrariastrum Sipman in Proc. Kon. Ned. Akad. Wetensch.,
Ser. C, Biol. Med. Sci. 83: 335. 1980 Type: C. ecua-
doriense (R. Sant.) Sipman in Proc. Kon. Ned. Akad.
Wetensch., Ser. C, Biol. Med. Sci. 83: 343. 1980 (Parme-
lia ecuadoriensis R. Sant. in Bot. Not. 1942: 328. 1942).
Diagnostic characters. – Lobes linearly elongate; conidia
cylindrical; apothecia with solid stipe.
Notes. – This genus was separated from Everniastrum,
which differs in having more regularly branched lobes, a hol-
low stipe, larger asci and a thinner hypothecium (Sipman,
1980, 1986). However, the distinction between the two genera
is disputed (Cu lber son & Cu lber s on, 1981). Additio nal da t a are
necessary to clarify their taxonomic status.
Everniastrum Hale ex Sipman in Mycotaxon 26: 237. 1986 –
Ty p e : E. cirrhatum (Fr.) Hale ex Sipman in Mycotaxon
26: 237. 1986 (Parmelia cirrhata Fr., Syst. Orb. Veg. 1:
283. 1825).
Diagnostic characters. – Lobes linearly elongate (Fig. 4J);
conidia bifusiform; apothecia with hollow stipe.
Notes. – The distinction of this genus from Cetrariastrum
requires further studies, as discussed above. This is a pan-
tropical genus with centers of distribution in the Neotropics
and Asia.
Hypotrachyna (Vain.) Hale in Phytologia 28: 340. 1974 – Type:
H. brasiliana (Nyl.) Hale in Phytologia 28: 340. 1974 (Par-
melia brasiliana Nyl in Flora 68: 611. 1885).
Diagnostic characters. – Lobes dichotomously branched,
with truncate apices (Fig. 4K); conidia bifusiform; rhizines
richly dichotomously branched.
Notes. – This pantropical genus is paraphyletic in its cur-
rent circumscription. Asian species with broad lobes were
shown to be unrelated and consequently separated as Remoto-
trachyna (Divakar & al., 2010). The classification of the re-
maining Hypotrachyna species needs to be addressed by a
study including more taxa and molecular characters.
Parmelinopsis Eli x & Hale in Mycot a xon 29: 242. 1987 – Type:
P. horrescens (Taylor) Eli x & Hale in Mycot axon 29: 242.
1987 (Parmelia horrescens Taylor in Mackay, Fl. Hiber n,
Part 2: 144. 1836).
Diagnostic characters. – Lobes dichotomously branched,
with truncate apices (Fig. 4L); conidia bifusiform or cylindri-
cal; rhizines simple to sparsely dichotomously branched.
Notes. – This pantropical to temperate genus is paraphy-
letic and nested within Hypotrachyna. Traditio nall y it ha s been
distinguished from Hypotrachyna based on the presence of
cilia and less richly branched rhizines. It remains to be seen
whether this genus can be kept separate from Hypotrachyna in
a modified circumscription or needs to be synonymized with
Hypotrachyna.
6. Parmeliopsis clade
This small clade includes only the genus Parmeliopsis, a
genus of six species. The phylogenetic placement of this clade
remains uncertain. It is unique among parmelioid lichens for
having richly branched conidiophores (Vobis, 1980).
Parmeliopsis (Nyl.) Nyl. in Not. Sällsk. Fauna Fl. Fenn. Förh.
8: 121. 1866 – Type: P. ambigua ( Wu l fen) Nyl ., Sy n. Meth.
Lich. 2: 54. 1869 (Lichen ambiguus Wulfen in Jacquin,
Collectanea 4: 239. 1790).
Diagnostic characters. – Lobes subirregular; pored epi-
cortex present; isolichenan; conidiophores branched; conidia
falcate.
7. Nipponoparmelia clade
This newly discovered clade includes a group of East
Asian species previously placed in Parmelia s.str. (Hale,
1987) that differs morphologically from other species in this
genus by having lateral, punctate pseudocyphellae. It was
later treated as a subgenus Nipponoparmelia within Parmelia
(Kurokawa, 1994). The subgenus is here raised to the generic
rank.
1749
Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
Nipponoparmelia (Kurok.) K.H. Moon, Y. Ohmura & Kashiw.
ex A. Crespo & al., s t at. n ov. [MB 516758] ≡ Parmelia
subg. Nipponoparmelia Kurok. in J. Jap. Bot. 69: 121.
1994 – Type: N. laevior (Nyl.) K.H. Moon, Y. Ohmura &
Kashiw. ex A. Crespo & al.
Diagnostic characters. – Lobes subirregular; non-pored
epicortex, punctiform pseudocyphellae present; conidia cy-
lindrical.
Notes. – This small East Asian genus is characterized by
marginal punctiform pseudocyphellae, grey to grey-brown
thalli and simple to furcate rhizines. The following four spe-
cies are included in the current circumscription of this genus.
Nipponoparmelia isidioclada (Vain.) K.H. Moon, Y. Ohmura
& Kashiw. ex A. Crespo & al., comb. nov. [MB MB516759]
Parmelia isidioclada Vain. in Bot. Mag. (Tokyo) 35:
48. 1921.
Nipponoparmelia laevior (Nyl.) K.H. Moon, Y. Ohmura &
Kashiw. ex A. Crespo & al., comb. nov. [MB MB516760]
Parmelia laevior Nyl., Lich. Jap.: 28. 1890.
Nipponoparmelia pseudolaevior (Asahina) K.H. Moon,
Y. Ohmura & Kashiw. ex A. Crespo & al., comb. nov.
[MB 516761] ≡ Parmelia pseudolaevior Asahina in J. Jap.
Bot. 26: 331. 1951.
Nipponoparmelia ricasolioides (Nyl.) A. Crespo & Divakar,
comb. nov. [MB 516762] Parmelia ricasolioides Nyl. in
Flora 70: 135. 1887.
8. Parmelia clade
This group is not strongly supported as monophyletic but
additional data are required to evaluate the relationships of
the genera listed here. Morphologically these genera are quite
dive r se and also include biogeog r aph ical ly dis t a nt entit ies, such
as the primarily northern hemispheric, temperate genus Parme-
lia and the tropical genera Relicina and Relicinopsis.
Parmelia Ach., Methodus: 153. 1803 – Type: P. saxatilis ( L .)
Ach., Methodus: 204. 1803 (Lichen saxatilis L., Sp. Pl. 2:
1142. 1753).
Diagnostic characters. – Lobes subirregular (Fig. 4M);
non-pored epicortex, effigurate to elongate pseudocyphellae
present; isolichenan; conidia cylindrical or bifusiform.
Notes. – Among the most surprising result of our analyses
was the polyphyly of Parmelia s.str. A group of East Asian taxa
with punctiform pseudocyphellae is segregated as Nippono-
parmelia (see above), whereas a predominantly Australasian
group of species related to P. signifera is tentatively kept in
Parmelia. However, relationships among these well-supported
groups are resolved only with short internodes, none of which
well-spported. This predominantly Australasian clade includes
species with usually broader lobes, but additional morphologi-
cal studies are needed in addition to a more extensive taxon
sampling and molecular characters, to better understand the
phylogeny of this clade. Parmelia in its restricted sense is a
small genus of temperate species, with a center of distribution
in the Northern Hemisphere.
Relicina (Hale & Kurok.) Hale in Phytologia 28: 484. 1974 –
Ty p e: Relicina eumorpha (Hepp) Hale in Phytologia 28:
484. 1974 (Parmelia eumorpha Hepp in Zollinger, Syst.
Verz.: 6, 9. 1854).
Diagnostic characters. – Lobes sublinear, subdichoto-
mously to dichotomously branched; pored epicortex present;
isolichenan; conidia bifusiform; cortex with usnic acid; bulbate
cilia present.
Notes. – This tropical genus has its center of species diver-
sity in eastern Asia and Australasia. It is similar to Bulbothrix
in having bulbate cilia, but differs from that genus in cortical
chemistry and conidia shape and is not closely related. An-
other similar genus is Relicinopsis, which primarily differs in
lacking bulbate cilia and having fusiform conidia. Our studies
indicate that the two genera are probably better regarded as
synonymous, since Relicinopsis is nested within Relicina in the
1GENE analysis. However, this relationship lacks support and
hence additional data are required before any nomenclatural
conclusion is reached.
Relicinopsis Eli x & Verdon in Myc otaxon 27: 281. 1986 – Typ e:
R. intertexta (Mont. & Bosch) Elix & Verdon in Myco-
taxon 27: 281. 1986 (Parmelia intertexta Mont. & Bosch.
in Mont., Syll. Gen. Sp. Crypt.: 327. 1856).
Diagnostic characters. – Lobes sublinear, subdichoto-
mously to dichotomously branched; pored epicortex present;
isolichenan; conidia elongate fusiform or cylindrical; cortex
with usnic acid; simple cilia present.
Notes. – The taxonomic status of this genus remains un-
certain, see under Relicina.
9. Melanohalea clade
This clade is expanded in comparison with its previous
circumscription (Blanco & al., 2006) to include also the Mel-
anelixia clade. Genera in this clade have a cell wall poly-
saccharide that has not yet been identified and may or may
not have a pored epicortex and/or pseudocyphellae. Neither
atranorin nor usnic acid is present as cortical compounds, but
species in this group contain melanoid substances that are
responsible for their brown color (Fig. 4N–O). The Melanelia
disjuncta group has not yet been assigned to a genus. The
group certainly is not related to M. stygia the type of Mel-
anelia, which is a cetrarioid genus. However, additional data
are necessary to evaluate whether this group can be placed
within one of the current genera in the Melanohalea clade or
whether a new genus needs to be described to accommodate
these taxa.
Emodomelanelia Divakar & A. Crespo, gen. nov. [M B 516763]
– Type: Emodomelanelia masonii (Es sl. & Poelt) Diva k ar
& A. Crespo, comb. nov. [MB 516764] Parmelia masonii
Essl. & Poelt in Bryologist 94: 203. 1991.
1750
TA XO N 59 (6) • December 2010: 1735–1753Crespo & al. • Generic classification of parmelioid lichens
Thallus laxe adnatus, pallide ad obscure brunneus; cum
pseudocyphellis marginalibus vel etiam laminalibus, albis;
soralia isidiaque desunt; superficies inferior nigra; cum rhi-
zinis simplicibus vel furcatis, nigris. Apothecia sessilia vel
substipitata, cum marginibus pseudocyphellatis; ascosporae
parietibus ca. 1–2 µm crassis. Conidia bifusiformia.
Diagnostic characters. – Thallus olive brown to brown;
lobes narrow to moderately broad; non-pored epicortex, ef-
figurate pseudocyphellae present; conidia bifusiform; cortex
HNO3+ green.
Etymology. – The epithet emodo refers to the Himalayas
and melanelia to brown color of the thallus upper surface.
Notes. – This new monospecific genus includes a parmeli-
oid species that combines characters typical for Parmelia s.str.,
such as laminal and marginal effigurate pseudocyphellae and
large ascospores, with characters typical of the brown parmeli-
oid genera, such as an olive-brown to brown upper surface and
lack of atranorin. When describing the new species, Esslinger &
Poelt (1991) pointed out that the placement in that genus was ten-
tative. The species is an Asian endemic, known from mainland
China, India, Nepal and Taiwan, where it is common on rocks
in subalpine to alpine habitats (Esslinger & Poelt, 1991; Ahti
& al., 1999; Ku rokawa & Lai, 2001; Divaka r & Upret i, 2005b).
Melanelixia O. Blanco & al. in Mycol. Res. 108: 881. 2004 –
Ty p e : M. glabra (Schaer.) O. Blanco & al. in Mycol. Res.
108: 882. 2004 (Parmelia olivacea α. corticola a. glabra
Schaer., Lich. Helv. Spic. 10: 466. 1840).
Diagnostic characters. – Lobes subirregular, plane to con-
cave; pored epicortex present; conidia cylindrical to fusiform;
cortex HNO3–.
Notes. – Melanelixia includes species occurring chiefly in
temperate regions of the Northern and Southern Hemispheres
that grow on bark and wood. It is characterized by having a
pored (fenestrate) epicortex, lacking pseudocyphellae and con-
taining lecanoric or gyrophoric acids as the primary medul-
lary constituent. It is similar to Pleurosticta, which differs in
having broader lobes, reticulated epicortical pores, a pigment
re actin g viole t in K and HNO3, and the presence of depsidones
in the medulla. Four species from the Southern Hemisphere,
which were previously placed here (Blanco & al., 2004a), but
were not formally transferred since they contain gyrophoric
acid rather than lecanoric acid like the Northern Hemisphere
taxa (Esslinger, 1977), have been included in the phylogenetic
analyses. They cluster with strong support as sister group to
Northern Hemisphere Melanelixia spp. Conse quently, they are
here transferred into Melanelixia.
Melanelixia calva (Essl.) A. Crespo, Divakar & Elix, comb.
nov. [MB 516765] ≡ Parmelia calva Essl. in J. Hattori Bot.
Lab. 42: 60. 1977 ≡ Melanelia calva (Essl.) Essl. in My-
cotaxon 7: 47. 1978.
Melanelixia glabratuloides (Es sl.) A. Cr espo, Divakar & Elix,
comb. nov. [MB 516766] ≡ Parmelia glabratuloides Essl.
in J. Hattori Bot. Lab. 42: 72. 1977 ≡ Melanelia glabratu-
loides (Essl.) Essl. in Mycotaxon 7: 48. 1978.
Melanelixia piliferella (Essl.) A. Crespo, Divakar & Elix,
comb. nov. [MB MB516767] ≡ Parmelia piliferella Essl.
in J. Hattori Bot. Lab. 42: 83. 1977 Melanelia piliferella
(Essl.) Essl. in Mycotaxon 7: 48. 1978.
Melanelixia subglabra (Räsänen) A. Crespo, Divakar & Elix,
comb. nov. [MB 516768] Parmelia subaurifera va r.
subglabra Räsänen in Ann. Bot. Soc. Zool.-Bot. Fenn.
Vanamo 2(1): 19. 1932 ≡ Parmelia subglabra (Räsänen)
Essl. in Bryologist 76: 307. 1973 ≡ Melanelia subglabra
(Räsänen) Essl. in Mycotaxon 7: 48. 1978.
Melanohalea O. Blanco & al. in Mycol. Res. 108: 882. 2004
– Type: M. exasperata (De Not.) O. Blanco & al. in My-
col. Res. 108: 882. 2004 (Parmelia exasperata De Not. in
Giorn. Bot. Ital. 2: 193. 1847).
Diagnostic characters. – Lobes subirregular, plane to
concave (Fig. 4 N); pseudocyphellae present, on tuberculae;
conidia elongate cylindrical to fusiform; cortex HNO3–.
Notes. – This genus is most common in the Northern Hemi-
sphere and includes species occurring on bark or wood. It is
characterized by pseudocyphellae, often on warts or isidial tips,
a nonpored epicortex, and a medulla containing depsidones or
lacking secondary compounds.
Pleurosticta Petr. in Kr y ptog. Forsch. 2: 190. 1931 – Type: P. li-
chenicola Petr. in Kryptog. Forsch. 2: 190. 1931 (= pycnidia
of Pleurosticta acetabulum (Neck.) Lumbsch & Elix in
Lumbsch, Kothe & Elix in Mycotaxon 33: 453. 1988)
Diagnostic characters. – Broad lobes (Fig. 4O); pored
epicortex present; isolichenan; conidia cylindrical to elongate
fusiform; cortex HNO3+ violet.
Notes. – This is a small genus of two species that is re-
stricted to Eurasia and North Africa. Its relationships with other
groups of brown parmelioid lichens requires further study.
Excluded genera and genera not studied
The following genera formerly placed in the parmelioid
group based on morphology (Elix, 1993; DePriest, 1999) belong
to other non-parmelioid groups: Allantoparmelia (Vain.) Essl.,
Arctoparmelia Hale, Everniopsis Nyl., Imshaugia S.L.F. Mey.,
Melanelia Essl., Omphalodium Meyen & Flot., Omphalora
T.H. Nash & Hafellner, and Psiloparmelia Hale. Everniop-
sis and Psiloparmelia were previously shown to belong to a
separate psiloparmelioid group within Parmeliaceae (Crespo &
al., 2007), while numerous studies have shown that Melanelia
s.str. belongs to the clade of cetrarioid lichens (Blanco & al.,
2004a, 2006; Thell & al., 2004, 2009; Crespo & al., 2007).
The placements of Allantoparmelia and Imshaugia wit h i n Par-
meliaceae remain uncertain (Thell & al., 2004; Crespo & al.,
2007), while Arctoparmelia has been shown to belong to the
hypogymnioid group (Crespo & al., 2007). Omphalodium and
Omphalora originated outside the parmelioid group (Thell &
al., 2002, 2004).
The species that include the types of the following ge-
neric names have not yet been studied by molecular methods
1751
Crespo & al. • Generic classification of parmelioid lichesTA XO N 59 (6) • December 2010: 1735–1753
Ahti, T., Lai, M.J. & Qian, Z.G. 1999. Notes on the lichen flora of
China: Parmeliaceae and Sphaerophoraceae. Fung. Sci. 14: 12 3
126.
Alstrup, V. & Hawksworth, D.L. 1990. The lichenicolous fungi of
Greenland. Meddel. Grønland, Biosci. 31: 1–90.
Amo, G., Crespo, A., Elix, J.A. & Lumbsch, H.T. 2010a. Ad d it ional
morphological diversity in Xanthoparmelia: Placoparmelia and
Omphalodiella belong to this monophyletic clade. Bryologist 113:
376–386.
Amo, G., Elix, J.A., Blanco, O., Lumbsch, H.T. & Crespo, A. 2010b.
The genus Karoowia (Par meliaceae, Ascomycota) includes un-
related clades nested within Xanthoparmelia. Austral. Syst. Bot.
23: 173–184.
Blanco, O., Crespo, A., Divakar, P.K., Elix, J.A. & Lumbsch, H.T.
2005. Molecular phylogeny of parmotremoid lichens (Ascomycota,
Parmeliaceae). Mycologia 97: 150–159.
Blanco, O., Crespo, A., Divakar, P.K., Esslinger, T.L., Hawksworth,
D.L. & Lumbsch, H.T. 2004a. Melanelixia and Melanohalea,
two new genera segregated from Melanelia (Parmeliaceae) based
on molecular and morphological data. Mycol. Res. 108: 873–884.
Blanco, O., Crespo, A., El ix, J.A., Hawksworth, D.L. & Lumbsch,
H.T. 2004b. A molecular phylogeny and a new classification of
parmelioid lichens containing Xanthoparmelia-t y pe li ch e nan (As -
comycota: Lecanorales). Taxon 53: 959–975.
Blanco, O., Crespo, A., Ree, R.H. & Lumbsch, H.T. 2006. Major
clades of parmeliold lichens (Par meliaceae, Ascomycota) and the
evolution of their morphological and chemical diversity. Molec.
Phylog. Evol. 39: 52–69.
and hence their placement and taxonomic status is unknown:
Bulborrhizina Kurok ., Parmotremopsis Elix & Hale, and Pseu-
doparmelia Lynge.
DISCUSSION
In this study we have gathered DNA sequence data avail-
able in GenBank and obtained 201 new sequences to address
the generic circumscriptions in all clades of parmelioid gen-
era. Our analyses identified eight well-supported major clades
within parmelioid lichens, the majority agreeing with the clades
found by Blanco & al. (2006). The exceptions include an en-
larged circumscription of the Parmelina clade to include taxa
previously placed in the Hypotrachyna clade and inclusion of
the Melanelixia clade in the enlarged Melanohalea clade. The
Cetrelia, Nipponoparmelia, Parmeliopsis clade s are he re newly
recognized. We attempted to keep nomenclatural changes at
a minimum. Although four clades were shown to be indepen-
dent and merit recognition at some taxonomic level, we only
proposed the acceptance of two new genera. One new genus
(Emodomelanelia) is described and a new combination into
Nipponoparmelia is made for species previously classified in
the highly polyphyletic genus Parmelia sensu Hale (1987 ). Eve n
after segregation of these two genera, Parmelia remains highly
polyphyletic. The Canoparmelia crozalsiana and Parmelia
signifera groups are shown to be unrelated to the species that
include the types of their generic names. However, we refrain
from describing new genera for those groups here, since our
understanding of the morphological characters to circumscribe
these clades is currently too poor. Additional taxonomic studies
are necessary before nomenclatural changes are made.
We also identified a number of remaining problems in
the generic classification of parmelioid lichens. These include
the circumscription of Parmotrema (especially the relation-
ships to the Canoparmelia crozalsiana group), the segrega-
tion of Bulbothrix into two clades with Parmelinella nested
within one of these clades, the distinction of Myelochroa and
Parmelina, the generic circumscription in the Hypotrachyna
clade (i.e., the polyphyly of Everniastrum, Hypotrachyna and
Parmelinopsis), polyphyly of Parmelia (with the Australasian
P. signifera probably representing a distinct lineage), the re-
lationships of Relicina and Relicinopsis, and the placement of
the Melanelia disjuncta group. Further, no molecular data are
available for the species that include the types of three generic
names (Bulborrhizina, Parmotremopsis, Pseudoparmelia).
Thus, our study has effectively focused forthcoming generic
level phylogenetic studies in this lichen group on these prob-
lematic generic groups.
Although a number of problems remain, significant prog-
ress in our understanding of the phylogeny of parmelioid li-
chens has been made during the last decade. The classification
of the family has now been put on a sound phylogenetic basis.
A few new genera have been described, while many others
have been synonymized. The taxonomic significance of mor-
phological and chemical characters at the generic level was
evaluated. Some vegetative characters, such as the presence of
cilia and rhizine-types, are shown to be too homoplasious and
hence of minor importance at the generic level for parmelioid
lichens. More changes in the generic classification will ensue
following additional studies directed at the problems identi-
fied here. Further, a major remaining problem is to resolve
the backbone relationships among major clades of parmelioid
lichens, which will require the sequencing of additional loci.
However, a stable framework for the generic classification has
been developed in this collaborative project. We hope that this
framework will assist lichenologists in the near future to refine
a generic classification of parmelioid lichens that ref lects the
phylogenetic relationships.
ACKNOWLEDGEMENTS
We wish to thank Allison Knight, Gary Perlmutter, Ken Sweat,
James Lendemer and Gennadii Urbanavichius for providing us with
fresh material for our studies. We thank John Porman n and Sean Dilda
from the Duke Shared Cluster Resource and Michael Nuhn from the
Nano+Bio Center for their support with installing and running the
necessary software. This study has been supported financially by
the Spanish Ministerio de Ciencia e Innovación (CGL2008-01125-E/
BOS, CGL2007-64652/BOS), and Ramon y Cajal grant (RYC02007-
01576) to PKD, a start up fund of The Field Museum to Thorsten
Lumbsch, the Swedish Research Cou ncil grants V R 629-2001-5756,
VR 621-2003-303 and VR 621-2006-3760 to Mats Wedin. We thank
th e Gal ap ago s Na tiona l Par k for permi ssion to anal yze thei r mat e ria l.
This is publication no. 2001 of the Charles Dar wi n Research Station.
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... belongs to the parmelioid crown of Parmeliaceae and includes c. 40 currently accepted species Molina et al. 2017). The genus is characterized by having a foliose thallus with simple to furcate and squarrose rhizines, a non-pored epicortex, effigurate to elongate pseudocyphellae on the upper surface, isolichenan, and cylindrical or bifusiform conidia (Crespo et al. 2010;Thell et al. 2012). Parmelia s. str. is a widespread genus in the Northern Hemisphere distributed in boreal-temperate Europe, North America and eastern Asia (Hale 1987;Hawksworth et al. 2008Hawksworth et al. , 2011Crespo et al. 2010). ...
... The genus is characterized by having a foliose thallus with simple to furcate and squarrose rhizines, a non-pored epicortex, effigurate to elongate pseudocyphellae on the upper surface, isolichenan, and cylindrical or bifusiform conidia (Crespo et al. 2010;Thell et al. 2012). Parmelia s. str. is a widespread genus in the Northern Hemisphere distributed in boreal-temperate Europe, North America and eastern Asia (Hale 1987;Hawksworth et al. 2008Hawksworth et al. , 2011Crespo et al. 2010). The Australasian species have been segregated in the genus Notoparmelia A. Crespo et al. (Ferencova et al. 2014) and previously some East Asian species with punctate pseudocyphellae at the lobe edges were accommodated in the genus Nipponoparmelia (Kurok.) ...
... The Australasian species have been segregated in the genus Notoparmelia A. Crespo et al. (Ferencova et al. 2014) and previously some East Asian species with punctate pseudocyphellae at the lobe edges were accommodated in the genus Nipponoparmelia (Kurok.) K. H. Moon et al. (Crespo et al. 2010). Within Parmelia s. str., the P. saxatilis group is a monophyletic clade that includes P. discordans Nyl., P. ernstiae Molina et al. 2017). ...