Phytotaxa 132 (1): 21–38 (2013)
www.mapress.com / phytotaxa /
Copyright © 2013 Magnolia Press
ISSN 1179-3155 (print edition)
Article
PHYTOTAXA
ISSN 1179-3163 (online edition)
http://dx.doi.org/10.11646/phytotaxa.132.1.2
A molecular perspective on generic concepts in the Hypotrachyna clade
(Parmeliaceae, Ascomycota)
PRADEEP K. DIVAKAR1, ANA CRESPO1, JANO NÚÑEZ-ZAPATA1, ADAM FLAKUS2, HARRIE J.M.
SIPMAN3, JOHN A. ELIX4, H. THORSTEN LUMBSCH5
1
Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, Madrid 28040, Spain;
email: pdivakar@farm.ucm.es, acrespo@farm.ucm.es
2
Laboratory of Lichenology, W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46, PL–31–512 Kraków, Poland
3
Botanischer Garten und Botanisches Museum Berlin-Dahlem, Freie Universität Berlin, Königin-Luise-Straße 6–8, 14195 Berlin,
Germany
4
Research School of Chemistry, Building 33, Australian National University, Canberra, ACT, Australia; email: john.elix@anu.edu.au
5
Science & Education, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605-2496, U.S.A.;
Email: tlumbsch@fieldmuseum.org
Abstract
Recently, molecular phylogenetic studies have revolutionized the generic concepts in Parmeliaceae and in lichen forming
fungi in general. In the present study, the generic delimitation in the Hypotrachyna clade is revised using a molecular
phylogeny of nuclear ITS, LSU and mitochondrial SSU rDNA sequences of 88 hypotrachynoid taxa. Morphological and
chemical features are also revised in each group. 118 sequences are newly generated for this study. Our phylogenetic
analyses show the polyphyly of Hypotrachyna as currently circumscribed which falls into four well-supported and one
unsupported clade. Cetrariastrum, Everniastrum and Parmelinopsis are nested within Hypotrachyna s. lat.,
Parmelinopsis being also polyphyletic and nested in one of the Hypotrachyna clades. Cetrariastrum is monophyletic but
clustered within Everniastrum. Two alternative hypotheses tests significantly rejected the monophyly of these three
genera. As a consequence, the genera Cetrariastrum, Everniastrum, and Parmelinopsis are reduced to synonymy with
Hypotrachyna. Furthermore, we here propose an alternative classification to recognize the well-supported clades at
subgeneric level and leave the remaining species unclassified within the genus. Five new subgenera are proposed:
Hypotrachyna subgen. Cetrariastrum, Hypotrachyna subgen. Everniastrum, Hypotrachyna subgen. Longilobae,
Hypotrachyna subgen. Parmelinopsis, and Hypotrachyna subgen. Sinuosae. Forty-nine new combinations are proposed.
Key words: generic classification, lichens, molecular systematics, parmelioid lichens, taxonomy
Introduction
Traditionally, the generic classification in lichenised fungi is based on morphological, anatomical and
chemical characters. In Parmeliaceae, morphology of vegetative thalli have traditionally played an important
role in circumscribing genera with a number of generic segregates being described over the last three decades
(Culberson & Culberson 1981; Elix 1993b; Elix & Hale 1987; Elix et al. 1986; Hale 1974a, 1974b, 1984,
1986a, 1986b; Krog 1982; Kurokawa 1991; Sipman 1980; Sipman 1986). However, in recent years a number
of taxonomic re-evaluations, mainly based on molecular phylogenies, have been proposed (Amo de Paz et al.
2010a; Amo de Paz et al. 2010b; Blanco et al. 2005; Blanco et al. 2004b; Crespo et al. 2010b; Crespo et al.
2007; Divakar et al. 2006; Divakar et al. 2010; Divakar et al. 2012; Thell et al. 2006; Wirtz et al. 2006). These
studies revealed that the taxonomic significance of phenotypical characters of the vegetative thallus was
overestimated in several groups. As a consequence, some former segregates were synonymized, such as
Rimeliella Kurokawa (1991: 1) within Canomaculina Elix & Hale (1987: 239); nine genera in
Accepted by Mohammad Sohrabi: 8 Aug. 2013; published: 18 Sept. 2013
21
Xanthoparmelia; Canomaculina, Concamerella Culberson & Culberson (1981: 307) and Rimelia Hale &
Fletcher (1990: 23) within Parmotrema Massalongo (1860: 248) (reviewed by Crespo et al. 2011; Thell et al.
2012). At the same time, molecular data have helped to discover previously unrecognized lineages (genera)
within the family Parmeliaceae. Examples include the genera Melanelixia Blanco et al. (2004a: 881),
Melanohalea Blanco et al. (2004a: 882) and Montanelia Divakar et al. (2012: 2022) as segregates of
Melanelia Esslinger (1978: 46) s. lat. (Blanco et al. 2004a; Divakar et al. 2012); Austroparmelina Crespo et al.
(2010a: 209) segregated from Parmelina Hale (1974a: 481). Lastly, Remototrachyna Divakar et al. (2010:
584) was segregated from Hypotrachyna Hale (1974b: 340) s. lat. (Divakar et al. 2010). All the
aforementioned segregates were based on molecular and morphological data.
A group of tropical parmelioid lichens with predominantly corticolous species, lacking pseudocyphellae,
and having a pored epicortex includes the genera Bulbothrix Hale (1974a: 479), Cetrariastrum Sipman (1980:
335), Everniastrum Hale ex Sipman (1986: 237), Hypotrachyna s. lat., Parmelinella Elix & Hale (1987: 241)
and Parmelinopsis Elix & Hale (1987: 242). These genera were included in the Hypotrachyna clade in
previous molecular studies (Blanco et al. 2006; Crespo et al. 2007; Divakar et al. 2006). However, in more
recent studies the genera Bulbothrix, Parmelinella and Remototrachyna were shown to be distantly related to
the other genera and placed in the Parmelina clade (Crespo et al. 2010b; Divakar et al. 2010). The genera
Cetrariastrum, Everniastrum, Hypotrachyna s. lat., and Parmelinopsis clustered together in the Hypotrachyna
clade, which is one of the larger major clades among parmelioid lichens (Parmeliaceae) (Crespo et al. 2010b;
Divakar et al. 2010). Within the Hypotrachyna clade, the genus Hypotrachyna is the largest with ca. 188
described species. It includes mainly tropical species growing in moderate to high altitude with a centre of
diversity in tropical America (Sipman et al. 2009). Hypotrachyna species are characterized by a pored
epicortex, narrow, sublinear to linear elongate lobes, with truncate apices; dichotomously branched rhizines,
oval-ellipsoid ascospores and bifusiform conidia (Divakar et al. 2001, 2010; Elix 1993b; Hale 1975).
Parmelinopsis (25 species), a pantemperate and pantropical genus is a segregate of the genus Parmelina (Elix
& Hale 1987). The genus is readily distinguished by having sublinear, narrow, apically truncate grey lobes,
simple cilia, and simple to weakly dichotomously branched rhizines; ellipsoid, relatively large ascospores and
cylindrical-bifusiform conidia. Everniastrum (40 species) is characterized by regularly dichotomously
branched lobes, apothecia with hollow stipe, relatively large asci and a thin hypothecium (Sipman 1980).
Cetrariastrum sensu Sipman (1980) is similar to the former genus, but distinguished by having irregularly
branched lobes, apothecia with solid stipe, smaller asci and a thicker hypothecium. Both genera, whose
distinction has been disputed (Culberson & Culberson 1981), share common characters, such as long, linear,
canaliculate lobes, long marginal cilia and both have a pantropical distribution (Sipman 1986).
The present study aims to clarify the phylogenetic positions of Cetrariastrum, Everniastrum and
Parmelinopsis and also test the hypothesis that the morphological characters have evolved independently
within the clade as adaptations to ecological conditions. To address these questions, we used three molecular
markers ITS, nuclear LSU and mitochondrial SSU rDNA, and analysed these data using Bayesian and
maximum likelihood approaches. We sampled specimens from all the continents of their distribution:
America, Africa, Asia, Australia and Europe. The morphological features of the species were also revised.
Materials and Methods
Taxon sampling:—Data matrices of 88 samples, representing 58 species of the Hypotrachyna clade (Crespo
et al. 2010b) were assembled using sequences of nuclear ITS, LSU and mitochondrial SSU rDNA. Two
species of Parmeliopsis were used as outgroup, since this genus has previously been shown to be closely
related to this clade (Crespo et al. 2010b). GenBank accession numbers and details of studied material are
shown in Table 1. The data sets include 122 sequences from previous publications by our group (Blanco et al.
2004a; Crespo et al. 2007; Divakar et al. 2006; Divakar et al. 2010; Lumbsch et al. 2008), five downloaded
from GenBank and 118 newly generated sequences.
22 •
Phytotaxa 132 (1) © 2013 Magnolia Press
DIVAKAR ET AL.
Molecular methods:—Small samples prepared from freshly collected and frozen specimens were ground
with sterile plastic pestles. Total genomic DNA was extracted using the DNeasy Plant Mini Kit (Qiagen,
Hilden, Germany) according to the manufacturer’s instructions but with slight modifications (Crespo et al.
2001). Dilutions of 1:10 of the total DNA were used for PCR amplifications of the ITS, nu LSU rDNA and mt
SSU rDNA regions. Primers, PCR and cycle sequencing conditions were the same as described previously
(Crespo et al. 2007; Divakar et al. 2005). Sequence fragments obtained were assembled with SeqMan 4.03
(DNAStar) and manually adjusted.
Sequence alignments:—We used the program MUSCLE (Edgar 2004) to align DNA sequences of 88
specimens (Table 1) for each data set separately. The program Gblocks v0.91b (Castresana 2000; Talavera &
Castresana 2007) was used to remove regions of alignment uncertainty, using options for a “less stringent”
selection on the Gblocks web server (http://molevol.cmima.csic.es/castresana/Gblocks_server.html).
Phylogenetic analyses:—The alignments were analyzed using maximum likelihood (ML) and a
Bayesian approach (B/MCMC). ML analyses were performed using an online version of the program RaxML
v7.0.4 ( http://phylobench.vital-it.ch/raxml-bb/; Stamatakis 2006; Stamatakis et al. 2008 ) for the partitioned
combined data set. We used the GTRGAMMA model, which includes a parameter (Γ) for rate heterogeneity
among sites and chose not to include a parameter for estimating the proportion of invariable sites (Stamatakis
2006; Stamatakis et al. 2008). The bootstrap analysis was run with 1000 pseudoreplicates.
Bayesian analyses were done using the program MrBAYES 3.1.2 (Huelsenbeck & Ronquist 2001).
Models of DNA sequence evolution for each locus were selected with the program jModeltestv0.1 (Posada
2008), using the Akaike information criterion (AIC; Akaike 1974). The concatenated three-loci data set was
partitioned as ITS, nuLSU and mtSSU, specifying the best fitting model, allowing unlinked parameter
estimation and independent rate variation. No molecular clock was assumed. Four parallel runs were made
with 4,000,000 generations starting with a random tree and employing 8 simultaneous chains each. Every
200th tree was saved into a file. The first 4000 trees were deleted as the “burn in” of the chains.
We used AWTY (Nylander et al. 2007) to compare splits frequencies in the different runs and to plot
cumulative split frequencies to insure that stationarity was reached. A majority rule consensus tree with
average branch lengths was calculated using the sumt option of MrBayes.
We used a ML approach to examine the heterogeneity in phylogenetic signal among the three data
partitions (Lutzoni et al. 2004). For the three loci and the concatenated analyses, the set of topologies reaching
≥70% bootstrap under likelihood was estimated. The combined data set topology was then compared for
conflict with ≥70% bootstrap intervals of the single gene analyses. If no conflict was evident, it was assumed
that the two data sets were congruent and could be combined.
Only clades that received bootstrap support above or equal 70% in ML analysis or posterior probabilities
equal or above 0.95 in MrBayes analysis were considered as well supported. Phylogenetic trees were drawn
using TREEVIEW (Page 1996).
Hypothesis testing:—The results of the phylogenetic analyses were incongruent with the current generic
classification in the Hypotrachyna clade. Hence we tested whether our data were sufficient to reject the
monophyly of currently accepted genera. For the hypothesis testing two different methods were employed: 1.
Shimodaira-Hasegawa (SH) test (Shimodaira & Hasegawa 1999) and 2. expected likelihood weight (ELW)
test (Strimmer & Rambaut 2002). The SH and ELW tests were performed using Tree-PUZZLE 5.2 (Schmidt
et al. 2002) with the combined data set on a sample of 200 unique trees, the best trees agreeing with the null
hypotheses, and the unconstrained ML tree. These trees were inferred in Tree-PUZZLE employing the
GTR+I+G nucleotide substitution model.
Morphological and chemical studies:—Thallus morphology was studied using a Leica Wild M 8
dissecting microscope for the measurement of lobe shape, size and width. All specimens included in the
molecular analysis were studied (see Table 1).
Chemical constituents were studied by thin layer chromatography using standardized methods (Culberson
1972; Culberson & Johnson 1982).
MOLECULAR PERSPECTIVE ON GENERIC CONCEPTS IN HYPOTRACHYNA
Phytotaxa 132 (1) © 2013 Magnolia Press
• 23
Results and Discussion
Phylogenetic studies:—A total of 34 new nuclear ITS, 43 new LSU rDNA and 41 new mitochondrial SSU
rDNA sequences were generated (Table 1). These were aligned with 122 sequences previously published by
us and five downloaded from GenBank (Table 1). The aligned matrix contained 453 unambiguously aligned
nucleotide position characters in ITS, 835 in nu LSU and 783 in mt SSU. The final alignment of combined
data set was 2071 positions in length, with 645 variable characters. The ITS PCR product obtained ranged
between 600 to 800 bp. Differences in size were due to the presence or absence of insertions of about 200 bp
identified as group I introns (Gutierrez et al. 2007) at the 3′ end of the SSU rDNA. We excluded group I
introns and 166 bp of the mtSSU and 47 bp of the ITS alignments from the analysis using GBlocks. GTR+G,
TIM1+I+G, and TIM1+I+G are resulted as best fit model of evolution for ITS, nu LSU and mt SSU
respectively. Topologies of single-locus analyses did not show conflict and hence combined analyses were
performed. Since the topologies of the ML and B/MCMC analyses did not show any supported conflict, only
the 50% majority-rule consensus tree of Bayesian tree sampling is shown with nodes in bold that received
strong support either in ML or Bayesian analyses (i.e. PP ≥0.95 in B/MCMC analysis and ML bootstrap
≥70%) (Fig. 1). B/MCMC posterior probabilities equal or above 0.95 are indicated above branches, while
values below branches are bootstrap support values of ML analysis.
TABLE 1. Specimens used in the study, with location, reference collection detail and GenBank accession numbers. Newly obtained
sequences for this study are in bold face. Missing data are indicated with dash (—).
Species
Locality
Collector(s)
Voucher
Specimens
GenBank accession numbers
ITS
mt SSU
nu LSU
Cetrariastrum andense
Peru: Ancash
Lumbsch, Wirtz & Ramírez
19334
F (MAF-Lich
15620)
GQ919269
GQ919217
GQ919245
C. dubitans
Peru: Ancash
Lumbsch, Wirtz & Ramírez
19366
F (MAF-Lich
15621)
GQ919270
GQ919217
GQ919246
C. ecuadoriense
Ecuador: Cotopaxi
Prov.
Palice s/n
HB. PALICE 3732
—
DQ287793
—
Everniastrum
cirrhatum 1
Costa Rica: San José
Trest 149
MAF-Lich 7465
AY611070
AY611128
AY607782
E. cirrhatum 2
Peru: Quebrada Parón
Lumbsch 19342r
MAF-Lich 13976
DQ279487
DQ287795
EU562674
E. lipidiferum
Peru: Quebrada Cojup
Lumbsch 19309b
MAF-Lich 13966
DQ279488
DQ287796
EU562675
E. nepalense
India: Uttarakhand
Divakar s/n
GUH 02-000924
AY611071
AY611129
AY607783
E. rhizodendroideum
China: Yunnan
Aptroot 55665
ABL
DQ279489
DQ287797
EU562676
E. sorocheilum
China: Yunnan
Crespo, Blanco & Argüello s/n
MAF-Lich 10375
DQ279490
DQ287798
EU562677
E. vexans
China: Yunnan
Aptroot 56597
ABL
DQ279491
DQ287799
EU562678
Hypotrachyna aff.
immaculata
China: Yunnan
Crespo, Blanco & Argüello s/n
MAF-Lich 10413
DQ279505
DQ287814
EU562680
H. aff. intercalanda
India: Tamil Nadu
Divakar, Upreti, Tandon &
Lumbsch 19733m
MAF-Lich
—
KF380962
KF380919
H. aff. oostingii
Chile: IX Región
Pérez-Ortega 325 DNA 2255
MAF-Lich
—
KF380963
KF380920
H. andensis 1
Bolivia: Camacho
Flakus & Rodríguez 17726
KRAM-L
—
KF380964
KF380921
H. andensis 2
Bolivia: Camacho
Flakus & Rodríguez 16907
KRAM-L
KF380886
KF380965
KF380922
H. aspera
Bolivia: Aniceto Arce
Flakus 18931
KRAM-L
KF380885
KF380966
KF380923
H. bogotensis 1
Peru: Cusco
Holgado, Mamani & Delgado
DNA 2199
MAF-Lich
KF380887
KF380967
KF380924
H. bogotensis 2
Chile: X Región
Pérez-Ortega 316 DNA 2254
MAF-Lich
KF380889
KF380969
KF380926
H. bogotensis 3
Bolivia: Camacho
Flakus & Rodríguez 17762
KRAM-L
KF380888
KF380968
KF380925
Hypotrachyna
booralensis
Australia:
Queensland
Lumbsch s/n
MAF-Lich 13969
DQ279493
DQ287801
EU562682
...... continued on the next page
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Phytotaxa 132 (1) © 2013 Magnolia Press
DIVAKAR ET AL.
TABLE 1 (continued)
Species
Locality
Collector(s)
Voucher
Specimens
GenBank accession numbers
ITS
mt SSU
nu LSU
H. brasiliana
Brazil: Municipio de
Piraquara
Sanders 99802.4
MAF-Lich 17019
—
DQ287802
—
H. britannica
Ireland: Kerry
Crespo & Gavilan s/n
MAF-Lich 15415
GQ919273
GQ919221
GQ919249
—
DQ912280
DQ912336
H. caraccensis 1
—
—
—
H. caraccensis 2
Bolivia: Nor Yungas
Flakus & Rodríguez 16878
KRAM-L
KF380890
KF380970
KF380927
H. chlorina 1
Ecuador: ZamoraChinchipe
Sipman 52924
BGO 0148626
KF380891
—
KF380928
H. chlorina 2
Bolivia: Nor Yungas
Flakus & Rodríguez 17120
KRAM-L
KF380892
KF380971
KF380929
H. dactylifera
Bolivia: Aniceto Arce
Flakus 18584
KRAM-L
KF380893
KF380972
KF380930
H. degelii 1
Bolivia: Aniceto Arce
Flakus & Quisbert 19849
KRAM-L
—
KF380973
KF380931
H. degelii 2
Bolivia: Nor Yungas
Flakus & Rodríguez 17261
KRAM-L
—
KF380974
KF380932
—
DQ912281
DQ912337
H. degelii 3
—
—
—
H. denshirrhizinata
Bolivia: Nor Yungas
Flakus & Rodríguez 17003
KRAM-L
—
KF380975
KF380935
H. dentella 1
Bolivia: Aniceto Arce
Flakus 18757
KRAM-L
KF380894
KF380976
KF380933
H. dentella 2
Bolivia: Aniceto Arce
Flakus 18528/1
KRAM-L
KF380895
KF380977
KF380934
H. enderythraea
Bolivia: Nor Yungas
Flakus & Rodríguez 17264
KRAM-L
—
KF380978
KF380936
H. endochlora 1
Great Britain: Scotland
Coppins s/n
MAF-Lich 10178
AY 611072
AY611130
AY607784
H. endochlora 2
Canary Island: Tenerife
Crespo s/n
MAF-Lich 10379
DQ279496
DQ287805
JN939614
H. endochlora 3
Bolivia: Aniceto Arce
Flakus & Quisbert 19892
KRAM-L
KF380896
KF380979
KF380937
H. endochlora 4
Bolivia: Aniceto Arce
Flakus 18577
KRAM-L
KF380897
KF380980
KF380938
H. fissicarpa
South Africa: W Cape
Crespo & al. s/n
MAF-Lich 13991
DQ279501
DQ287810
—
H. halei 1
Bolivia: Nor Yungas
Flakus & Rodriguez 16897
KRAM-L
KF380898
KF380981
KF380939
H. halei 2
Bolivia: Nor Yungas
Flakus & Rodríguez 16331
KRAM-L
KF380899
—
KF380940
H. imbricatula 1
Costa Rica: Manzanillo
Molina s/n
MAF-Lich 10382
DQ279502
DQ287811
GQ919253
H. imbricatula 2
South Africa: W Cape
Crespo & al. s/n
MAF-Lich 13990
DQ279503
DQ287812
EU562686
H. imbricatula 3
Bolivia: Nor Yungas
Flakus & Rodríguez 17234
KRAM-L
KF380900
KF380982
KF380941
H. imbricatula 4
Brazil: São Paulo
Benatti & Cintra 3159
SP
KF380901
KF380983
KF380942
H. immaculata
Australia: Queensland
Louwhoff, Molina & Elix s/n
MAF-Lich 7462
AY611073
AY611131
AY607785
H. intercalanda
Brazil: São Paulo
Benatti & Cintra 3209
SP
KF380902
KF380984
KF380943
H. laevigata 1
Great Britain: Scotland
Coppins s/n
MAF-Lich 10177
AY611074
AY611132
AY607786
H. laevigata 2
Bolivia: Nor Yungas
Flakus & Rodríguez 16952
KRAM-L
KF380903
KF380985
KF380944
H. livida 1
Brazil: São Paulo
Benatti & Cintra 3211
SP
KF380904
KF380986
KF380945
H. livida 2
Bolivia: Aniceto Arce
Flakus 18756
KRAM-L
KF380905
KF380987
KF380946
H. livida 3
Bolivia: Aniceto Arce
Flakus & Quisbert 19785
KRAM-L
KF380906
KF380988
KF380947
H. longiloba 1
Peru: Cusco
Holgado, Mamani & Delgado
DNA 2198
MAF-Lich
KF380907
KF380989
KF380948
H. longiloba 2
Bolivia: Nor Yungas
Flakus & Rodríguez 16333
KRAM-L
KF380908
KF380990
KF380949
H. microblasta
Bolivia: Nor Yungas
Flakus & Rodríguez 16970
KRAM-L
KF380909
KF380991
KF380950
H. neodissecta
South Africa: W Cape
Crespo & al. s/n
MAF-Lich 13986
DQ279510
DQ287820
EU562689
H. osseoalba
China: Yunnan
Crespo, Blanco & Argüello s/n
MAF-Lich 10390
DQ279512
DQ287822
EU562690
H. partita 1
Bolivia: Nor Yungas
Flakus & Rodríguez 16863
KRAM-L
—
KF380992
KF380951
H. partita 2
Bolivia: Camacho
Flakus & Rodríguez 17699
KRAM-L
KF380910
KF380993
KF380952
H. physcioides 1
China: Yunnan
Crespo, Blanco & Argüello s/n
MAF-Lich 10391
DQ279513
DQ287823
EU562691
...... continued on the next page
MOLECULAR PERSPECTIVE ON GENERIC CONCEPTS IN HYPOTRACHYNA
Phytotaxa 132 (1) © 2013 Magnolia Press
• 25
TABLE 1 (continued)
Species
Locality
H. physcioides 2
Collector(s)
Bolivia: Nor Yungas
Voucher
Specimens
Flakus & Rodríguez 16860
KRAM-L
GenBank accession numbers
ITS
mt SSU
nu LSU
KF380911
KF380994
KF380953
H. pluriformis
Bolivia: Aniceto Arce
Flakus & Quisbert 19784
KRAM-L
KF380912
KF380995
KF380954
H. polydactyla
Kenya: W province
Divakar & Lumbsch s/n
MAF-Lich 15518
GQ919283
GQ919231
GQ919258
H. prolongata
Bolivia: Nor Yungas
Flakus & Rodríguez 17011
KRAM-L
KF380913
KF380996
KF380955
H. pseudosinuosa 1
China: Yunnan
Crespo, Blanco & Argüello s/n
MAF-Lich 10392
DQ279516
DQ287826
EU562692
H. pseudosinuosa 2
China: Yunnan
Crespo, Blanco & Argüello s/n
MAF-Lich 10393
DQ279517
DQ287827
GQ919257
H. pulvinata
Mexico: Jalisco
Nash III 46756
ASU
KF380914
KF380997
KF380956
H. reducens
Costa Rica: Nat. Park
Irazú
Lücking 15450
F
DQ279520
DQ287830
—
H. revoluta
Spain: Puerto Urkiola,
Vizcaya
Noya & Olea s/n
MAF-Lich 6047
AY611075
AF351166
AY607787
H. rockii 1
Peru: Quebrada Parón
Lumbsch 19342l
MAF-Lich 13965
DQ279524
DQ287834
EU562693
H. rockii 2
Bolivia: Nor Yungas
Flakus & Rodríguez 16446/4
KRAM-L
KF380915
KF380998
KF380957
H. showmanii 1
USA: Pennsylvania
Lendemer 18060
NY 01080325
KF380916
KF380999
KF380958
H. showmanii 2
USA: Pennsylvania
Lendemer & Macklin s/n
HB. LENDEMER
2386 (MAF-Lich
15618)
GQ919287
GQ919234
—
H. sinuosa 1
Great Britain: Scotland
Coppins s/n
MAF-Lich 10179
AY611076
AY611133
AY607788
H. sinuosa 2
Chile: X Región
Pérez-Ortega 323 DNA 2252
MAF-Lich
—
KF381000
KF380959
H. steyermarkii 1
Bolivia: Aniceto Arce
Flakus & Quisbert 19701
KRAM-L
KF380917
KF381001
KF380960
H. steyermarkii 2
Bolivia: Nor Yungas
Flakus & Rodriguez 16864
KRAM-L
KF380918
KF381002
KF380961
H. taylorensis
Great Britain: Scotland
Hawksworth s/n
MAF -Lich 9921
AY581061
AY582298
AY578924
Parmelinopsis
afrorevoluta 1
Australia: New South
Wales
Elix 28562
Elix (MAF-Lich
15619)
GQ919286
GQ919233
GQ919259
P. afrorevoluta 2
Canary Island: Tenerife
Crespo s/n
MAF-Lich 10409
DQ279529
DQ287839
EU562681
P. cryptochlora
China: Yunnan
Crespo, Blanco & Arguello s/n
MAF-Lich 10398
DQ279535
DQ287845
EU562695
P. horrescens
Spain: La Coruña
Carvallal s/n
MAF-Lich 9913
AY581085
AY582321
AY578951
P. minarum
Spain: Cádiz
Crespo & al. s/n
MAF-Lich 7639
AY581086
AY582322
AY579852
P. neodamaziana
Australia: Queensland
Louwhoff, Molina & Elix s/n
MAF-Lich 10182
AY611107
AY611166
AY607820
P. subfatiscens 1
Australia: Queensland
Louwhoff, Molina & Elix s/n
MAF-Lich 6878
AY611108
AF351174
AY607821
Parmelinopsis
subfatiscens 2
China: Yunnan
Crespo, Blanco & Argüello s/n
MAF-Lich 10380
DQ279498
DQ287807
EU562684
—
AF410829
EU562698
AY607822
MAF -Lich 10181
AY611109
AY611167
AY607823
Parmeliopsis ambigua
—
Parmeliopsis hyperopta Spain: Madrid
—
Blanco s/n
The best tree under likelihood had a likelihood value of ln -15002.199. In the B/MCMC analysis, the
likelihood parameters in the sample had the following mean (Variance): LnL = -15045.533 (0.356), the
gamma shape parameter alpha = 0.312 (0.002) and pinvar = 0.496 (0.002).
The currently accepted genera Everniastrum, Hypotrachyna and Parmelinopsis are not monophyletic,
with Everniastrum and Hypotrachyna being paraphyletic, and Parmelinopsis polyphyletic. Cetrariastrum is
monophyletic but clustered within Everniastrum and this clade is nested within Hypotrachyna s.lat.
Monophyly of these three genera was rejected by the two alternative hypothesis tests (p<0.001 in all cases).
This clearly indicates that the current generic concept in the Hypotrachyna clade does not reflect phylogenetic
relationships and this is consistent with previous studies (Blanco et al. 2006; Crespo et al. 2010b; Crespo et al.
2007; Divakar et al. 2006; Lumbsch et al. 2008).
26 •
Phytotaxa 132 (1) © 2013 Magnolia Press
DIVAKAR ET AL.
FIGURE 1. 50% majority-rule consensus tree of the molecular phylogenetic relationships in the Hypotrachyna clade, based on 64000
trees from a B/MCMC tree-sampling procedure of a combined dataset of ITS, nu LSU, and mt SSU sequences. Two species of
Parmeliopsis used as outgroup. Posterior probabilities ≥ 0.95 are given above the branches, and values below the branches are ML
bootstrap values ≥ 70%. Branches that received strong support in any of the two analyses (RaxML and B/MCMC) are in boldface.
Asterisk mark shows the type species of the genus Hypotrachyna. Clades numbered indicate phylogenetic clusters explained in the
text.
MOLECULAR PERSPECTIVE ON GENERIC CONCEPTS IN HYPOTRACHYNA
Phytotaxa 132 (1) © 2013 Magnolia Press
• 27
Several well supported clades can be found within the Hypotrachyna clade. Clade 1 is sister to the
remaining species of the clade. It includes H. fissicarpa, endemic to east and south Africa, and the H.
longiloba group that includes species with separate, linear lobes, a densely rhizinate lower surface, and
containing atranorin and alectoronic, α- and β- collatolic, gyrophoric or anziaic acids. Hypotrachyna
fissicarpa, however, has short, sublinear, imbricate lobes, a moderately rhizinate lower surface and contains
atranorin and protocetraric acid. Species with similar morphology and chemistry can be found in other clades,
such as clade 5 (Hypotrachyna s. str.), and the unsupported clade (Fig. 1).The sister-group of clade 1 is wellsupported and consists of two major groups, only one of them, however, receives strong support. The latter
consists of clade 2 and a number of species currently placed in Hypotrachyna which form an unsupported
sister-group to clade 2. Clade 2 mostly includes species with separate, linear lobes and a densely rhizinate
lower surface, similar to species of clade 1. However, taxa in clade 2 contain usnic acid in the cortex, rarely
accompanied by atranorin. Hypotrachyna microblasta (Vain.) Hale (1975: 47) differs morphologically by
having short, sublinear lobes, but agrees with the other species in clade 2 in having a densely rhizinate lower
surface and containing usnic acid. The species in the unsupported sister-group of clade 2 are morphologically
and chemically similar to Hypotrachyna s.str. [clade 5, with type species H. brasiliana (Nyl.) Hale (1974b:
341)], but only distantly related to that clade. Clade 3 includes species of the genus Cetrariastrum and
Everniastrum lipidiferum (Hale & Wirth) Hale ex Sipman (1986: 241). Cetrariastrum has been distinguished
from Everniastrum based on an irregular branching pattern of the lobes, smaller asci, thicker hypothecium in
Cetrariastrum, and a different apothecial stalk (Sipman 1986). Clade 4 includes all species currently placed in
the genus Everniastrum, with the exception of E. lipidiferum. Hypotrachyna s.str. is the well supported clade
5. This clade and clade 6 have a well-supported sister-group relationship. Clade 6 includes species currently
placed in Hypotrachyna and Parmelinopsis. The latter genus has traditionally been separated from
Hypotrachyna based on the presence of cilia and less richly branched rhizines, characters that are regarded as
species-specific but unreliable at higher rank in other groups of parmelioid lichens, such as Parmotrema
(Divakar & Upreti 2005; Elix 1994; Krog & Swinscow 1981).
Characters, such as elongate lobes or presence of usnic acid, have evolved several times independently
within the Hypotrachyna clade, suggesting that they have an adaptive value in certain habitats. The
traditionally accepted genera in the Hypotrachyna clade were almost entirely circumscribed based on
characters of the vegetative thallus, with the exception of the genus Cetrariastrum. Vegetative characters have
repeatedly shown to be highly plastic in various groups of lichenized fungi (Högnabba 2006; Lumbsch et al.
2010; Parnmen et al. 2010; Stenroos & DePriest 1998; Tehler & Irestedt 2007). Thus it is not surprising that
the morphology-based genera within the Hypotrachyna clade were not confirmed by our phylogenetic
analysis.
Taxonomic conclusions:—Based on our phylogenetic analysis, we propose to reduce the genera
Cetrariastrum, Everniastrum, and Parmelinopsis to synonymy with Hypotrachyna. An alternative
classification would recognize all well-supported clades at generic level. This, however, would require the
description of additional new genera that would be difficult to circumscribe phenotypically, and further, would
leave the bulk of Hypotrachyna s.lat. species (sister-group to clade 2, Fig. 1) in an unresolved position. As an
alternative, we propose here to recognize the well-supported clades at subgeneric level and leave the
remaining species unclassified within the genus. Recognition at the subgeneric level also has the advantage
that monophyletic lineages that are clustered within the paraphyletic Hypotrachyna s. lat. can be recognized
without producing paraphyletic taxa (Hörandl & Stuessy 2010). We propose to recognize the H. longiloba
group in clade 1 as Hypotrachyna subgen. Longilobae, clade 2 as Hypotrachyna subgen. Sinuosae, clade 3 as
Hypotrachyna subgen. Cetrariastrum, clade 4 as Hypotrachyna subgen. Everniastrum, and clade 6 as
Hypotrachyna subgen. Parmelinopsis. As a consequence of the revised generic concept of Hypotrachyna,
several new subgenera need description and new combinations are necessary, and these are proposed below.
28 •
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DIVAKAR ET AL.
New subgenera:
Hypotrachyna subgen. Cetrariastrum (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. et stat.
nov. MycoBank No.: MB 803542
Cetrariastrum Sipman (1980: 335). Type species:—Hypotrachyna ecuadoriensis (R. Sant.) Divakar et al. (2013: 21–38);
Cetrariastrum ecuadoriense (R. Sant.) Sipman (1980: 343). Parmelia ecuadoriensis Santesson (1942: 328).
A subgenus in the genus Hypotrachyna, corresponding to clade 3 in Fig. 1, including all species placed in
Cetrariastrum by Sipman (1980, 1986) plus Everniastrum lipidiferum. The latter is included provisionally
because it appears more distantly related to the other species.
Hypotrachyna subgen. Everniastrum (Hale ex Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch,
comb. et stat. nov. MycoBank No.: MB 803543
Everniastrum Hale ex Sipman (1986: 335). Type species:—Hypotrachyna cirrhata (Fr.) Divakar et al. (2013: 21–38);
Everniastrum cirrhatum (Fr.) Hale ex Sipman (1986: 337). Parmelia cirrhata Fries (1825: 283).
A subgenus in the genus Hypotrachyna, corresponding to clade 4 in Fig. 1, including all species placed in
Everniastrum by Sipman (1980, 1986) excluding Everniastrum lipidiferum.
Hypotrachyna subgen. Longilobae Divakar, A. Crespo, Sipman, Elix & Lumbsch, subgen. nov. MycoBank
No.: MB 803544
Type species:—Hypotrachyna longiloba (H. Magn.) Smith (1993: 328). Parmelia longiloba Magnusson (1941: 7).
A new subgenus in the genus Hypotrachyna, corresponding to clade 1 (excl. H. fissicarpa) in Fig. 1,
characterized by separate, linear lobes, densely rhizinate lower surface and the presence of atranorin,
alectoronic, anziaic, α- and β-collatolic, and gyrophoric acids. All species included are distributed at higher
elevation mainly in the Neotropics, but also in the southern United States and East Africa.
Hypotrachyna subgen. Parmelinopsis (Elix & Hale) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. et
stat. nov. MycoBank No.: MB 803545
Parmelinopsis Elix & Hale (1987: 242). Type species:—Hypotrachyna horrescens (Taylor) Krog & Swinscow (1987:
420); Parmelinopsis horrescens (Taylor) Elix & Hale (1987: 242). Parmelia horrescens Taylor in Mackay (1836:
144).
A subgenus in the genus Hypotrachyna, corresponding to clade 6 in Fig. 1, including all species currently
placed in Parmelinopsis plus Hypotrachyna species with sparsely dichotomously branched rhizines, and
containing gyrophoric, lecanoric and olivetoric acids in the medulla.
Hypotrachyna subgen. Sinuosae Divakar, A. Crespo, Sipman, Elix & Lumbsch, subgen. nov. MycoBank
No.: MB 803546
Type species:—Hypotrachyna sinuosa (Sm.) Hale (1975: 63). Lichen sinuosus Smith (1809: tab. 2050).
A new subgenus in the genus Hypotrachyna, corresponding to clade 2 in Fig. 1, characterized by combination
of features in having mostly separate, linear lobes, densely rhizinate lower surface and the presence of usnic
acid, galbinic, norstictic, stictic and salazinic acids. All species included are mainly distributed at higher
elevation.
MOLECULAR PERSPECTIVE ON GENERIC CONCEPTS IN HYPOTRACHYNA
Phytotaxa 132 (1) © 2013 Magnolia Press
• 29
New combinations
Subgenus Cetrariastrum:
Hypotrachyna dubitans (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803547
Cetrariastrum dubitans Sipman (1980: 342).
Hypotrachyna ecuadoriensis (R. Sant.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803548
Parmelia ecuadoriensis Santesson (1942: 328); Cetrariastrum ecuadoriense (R. Sant.) Sipman (1980: 347).
Hypotrachyna kaernefeltii Divakar, A. Crespo, Sipman, Elix & Lumbsch, nom. nov. MycoBank No.: MB
803549
pro Cetrariastrum andense Kärnef. in Culberson & Culberson (1981: 297); Everniastrum andense Kärnefelt (1980:
387), nom. inval. (Art. 43.1.); non Hypotrachyna andensis Hale (1975: 23).
Hypotrachyna lipidifera (Hale & M. Wirth) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803550
Parmelia lipidifera Hale & M. Wirth (1971: 37); Cetrariastrum lipidiferum (Hale & M. Wirth) Culberson & Culberson
(1981: 287); Everniastrum lipidiferum (Taylor) Hale ex Sipman (1986: 241).
Subgenus Everniastrum:
Hypotrachyna africana (Hale) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803551
Cetrariastrum africanum Hale in Culberson & Culberson (1981: 296); Everniastrum africanum (Hale) Sipman (1986:
239).
Hypotrachyna alectorialica (W.L. Culb. & C.F. Culb.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb.
nov. MycoBank No.: MB 803552
Cetrariastrum alectorialicum Culberson & Culberson (1981: 297); Everniastrum alectorialicum (W.L. Culb. & C.F.
Culb.) Sipman (1986:239).
Hypotrachyna americana (Meyen & Flot.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803553
Evernia americana Meyen & Flotow (1843: 211); Cetrariastrum americanum (Meyen & Flot ) Culberson & Culberson
(1981: 305); Everniastrum americanum (Meyen & Flot.) Hale ex Sipman (1986: 239).
Hypotrachyna angolensis (W.L. Culb. & C.F. Culb.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb.
nov. MycoBank No.: MB 803554
Cetrariastrum angolense Culberson & Culberson (1981: 299); Everniastrum angolense (W.L. Culb. & C.F. Culb.)
Sipman (1986: 239).
Hypotrachyna arsenei (Hale & M. Wirth) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803555
Parmelia arsenei Hale & M. Wirth (1971: 40); Cetrariastrum arsenei (Hale & M. Wirth) Culberson & Culberson (1981:
300); Everniastrum arsenei (Hale & M. Wirth) Sipman (1986: 239).
Hypotrachyna arvidssonii (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803595
Everniastrum arvidssonii Sipman (1986: 243).
30 •
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DIVAKAR ET AL.
Hypotrachyna billingsii (W.L. Culb. & C.F. Culb.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803556
Cetrariastrum billingsii Culberson & Culberson (1981: 305); Everniastrum billingsii (W.L. Culb. & C.F. Culb.) Sipman
(1986: 239).
Hypotrachyna catawbiensis (Degel.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803557
Parmelia sorocheila var. catawbiensis Degelius (1941: 64); Cetrariastrum catawbiense (Degel.) Culberson & Culberson
(1981: 281); Everniastrum catawbiense (Degel.) Hale ex Sipman (1986: 237).
Hypotrachyna chilensis (Kurok.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803558
Cetrariastrum chilense Kurokawa (1999: 252).
Hypotrachyna cirrhata (Fr.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.: MB
803559
Parmelia cirrhata Fries (1825: 283); Cetrariastrum cirrhatum (Fr.) Culberson & Culberson (1981: 283); Everniastrum
cirrhatum (Fr.) Hale ex Sipman (1986: 237).
Hypotrachyna columbiensis (Zahlbr.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803560
Parmelia columbiensis Zahlbruckner (1929: 61); Cetrariastrum columbiense (Zahlbr.) Culberson & Culberson (1981:
285); Everniastrum columbiense (Zahlbr.) Hale ex Sipman (1986: 239).
Hypotrachyna constictovexans (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803561
Everniastrum constictovexans Sipman in Lumbsch et al. (2011: 53).
Hypotrachyna diffractaica (Y.M. Jiang & J.C. Wei) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb.
nov. MycoBank No.: MB 803562
Everniastrum diffractaicum Jiang & Wei (1993: 58).
Hypotrachyna fragilis (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803563
Everniastrum fragile Sipman (1986: 240).
Hypotrachyna latiloba (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803564
Everniastrum latilobum Sipman (1986: 243).
Hypotrachyna limiformis (Taylor) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803565
Parmelia limiformis Taylor (1847: 170); Cetrariastrum limiforme (Taylor) Culberson & Culberson (1981: 286);
Everniastrum limiforme (Taylor) Hale ex Sipman (1986: 240).
Hypotrachyna mexicana (Egan) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803566
Cetrariastrum mexicanum Egan in Culberson & Culberson (1981: 287); Everniastrum mexicanum (Egan) Sipman (1986:
241).
Hypotrachyna neocirrhata (Hale & M. Wirth) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803567
MOLECULAR PERSPECTIVE ON GENERIC CONCEPTS IN HYPOTRACHYNA
Phytotaxa 132 (1) © 2013 Magnolia Press
• 31
Parmelia neocirrhata Hale & Wirth (1971: 37); Cetrariastrum neocirrhatum (Hale & M. Wirth) Culberson & Culberson
(1981: 289); Everniastrum neocirrhatum (Hale & M. Wirth) Hale ex Sipman (1986: 241).
Hypotrachyna neohalei Divakar, A. Crespo, Sipman, Elix & Lumbsch, nom. nov. MycoBank No.: MB
803568
pro Cetrariastrum halei Culberson & Culberson (1981: 301); Everniastrum halei (W.L. Culb. & C.F. Culb.) Sipman
(1986: 240); non Hypotrachyna halei Sipman et al. (2009: 76).
Hypotrachyna neotropica Divakar, A. Crespo, Sipman, Elix & Lumbsch, nom. nov. MycoBank No.: MB
803569
pro Cetrariastrum peruvianum Hale in Culberson & Culberson (1981: 291); Everniastrum peruvianum (Hale) Sipman
(1986: 241); non Hypotrachyna peruviana (Nyl.) Hale (1975: 54).
Hypotrachyna nepalensis (Taylor) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803570
Parmelia nepalensis Taylor (1847: 172); Cetrariastrum nepalense (Taylor) Culberson & Culberson (1981: 301);
Everniastrum nepalense (Taylor) Hale ex Sipman (1986: 241).
Hypotrachyna nigrociliata (de Lesd.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803571
Parmelia nigrociliata Bouly de Lesdain (1933: 117); Cetrariastrum nigrociliatum (de Lesd.) Culberson & Culberson
(1981: 290); Everniastrum nigrociliatum (Taylor) Hale ex Sipman (1986: 241).
Hypotrachyna plana (Sipman) Divakar, A. Crespo, Elix & Lumbsch, comb. nov. MycoBank No.: MB 803594
Everniastrum planum Sipman (1980: 349)
Hypotrachyna pseudonepalensis (Hale & M. Wirth) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb.
nov. MycoBank No.: MB 803572
Parmelia pseudonepalensis Hale & Wirth (1971: 40); Cetrariastrum pseudonepalense (Hale & M. Wirth) Culberson &
Culberson (1981: 303); Everniastrum pseudonepalense (Hale & M. Wirth) Hale ex Sipman (1986: 242).
Hypotrachyna rhizodendroidea (J.C. Wei & Y.M. Jiang) Divakar, A. Crespo, Sipman, Elix & Lumbsch,
comb. nov. MycoBank No.: MB 803573
Cetrariastrum rhizodendroideum Wei & Jiang (1982: 496); Everniastrum rhizodendroideum (J.C. Wei & Y.M. Jiang)
Sipman (1986: 242).
Hypotrachyna scabrida (Elix & Pooprang) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803574
Everniastrum scabridum Elix & Pooprang in Pooprang et al. (1999: 112).
Hypotrachyna sinensis (J.B. Chen & J.C. Wei) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803575
Everniastrum sinense J.B. Chen & J.C. Wei in Chen et al. (1989: 434).
Hypotrachyna sorocheila (Vain.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803576
Parmelia sorocheila Vainio (1899: 123); Cetrariastrum sorocheilum (Vain.) Culberson & Culberson (1981: 292);
Everniastrum sorocheilum (Vain.) Hale ex Sipman (1986: 242).
Hypotrachyna subnepalensis (Hale) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803577
Cetrariastrum subnepalense Hale in Culberson & Culberson (1981: 304); Everniastrum africanum (Hale) Sipman (1986:
242).
32 •
Phytotaxa 132 (1) © 2013 Magnolia Press
DIVAKAR ET AL.
Hypotrachyna subplana (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803578
Everniastrum subplanum Sipman (1986: 244); Cetrariastrum subplanum (Sipman) Kurokawa (1999: 254).
Hypotrachyna subsorocheila (Y.M. Jiang & J.C. Wei) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb.
nov. MycoBank No.: MB 803579
Everniastrum subsorocheilum Jiang & Wei (1989: 246).
Hypotrachyna subvexans (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803580
Everniastrum subvexans Sipman (1986: 246).
Hypotrachyna vexans (Zahlbr. ex W.L. Culb. & C.F. Culb.) Divakar, A. Crespo, Sipman, Elix & Lumbsch,
comb. nov. MycoBank No.: MB 803581
Cetrariastrum vexans Zahlbr. ex Culberson & Culberson (1981: 294); Everniastrum vexans (Zahlbr. ex W.L. Culb. &
C.F. Culb.) Hale ex Sipman (1986: 242).
Subgenus Parmelinopsis:
Hypotrachyna bonariensis (Adler & Elix) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803582
Parmelinopsis bonariensis Adler & Elix (1987: 341).
Hypotrachyna cleefii (Sipman) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803583
Parmelina cleefii Sipman (1980: 352); Parmelinopsis cleefii (Sipman) V. Marcano & Sipman in Marcano et al. (1996:
214).
Hypotrachyna ectypa (Brusse) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803584
Parmelia ectypa Brusse (1991: 164); Parmelinopsis ectypa (Brusse) DePriest & Hale (1998: 203).
Hypotrachyna expallida (Kurok.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803585
Parmelia expallida Kurokawa (1968: 191); Parmelina expallida (Kurok.) Hale (1974a: 482); Parmelinopsis expallida
(Kurok.) Elix & Hale (1987: 242).
Hypotrachyna heteroloba (Zahlbr.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803586
Parmelia heteroloba Zahlbruckner (1909: 171); Parmelina heteroloba (Vain.) Hale (1974a: 482); Parmelinopsis
heteroloba (Vain.) Elix & Hale (1987: 242).
Hypotrachyna jamesii (Hale) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.: MB
803587
Parmelia jamesii Hale (1972: 179); Parmelina jamesii (Hale) Hale (1976: 35); Parmelinopsis jamesii (Hale) Elix & Hale
(1987: 242).
Hypotrachyna megadactyla (Aptroot) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank
No.: MB 803588
Parmelinopsis megadactyla Aptroot (1991: 242).
MOLECULAR PERSPECTIVE ON GENERIC CONCEPTS IN HYPOTRACHYNA
Phytotaxa 132 (1) © 2013 Magnolia Press
• 33
Hypotrachyna microlobulata (D.D. Awasthi) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803589
Parmelia microlobulata Awasthi (1976: 182); Parmelinopsis microlobulata (D.D. Awasthi) Elix & Hale (1987: 242).
Hypotrachyna nagalandica (K. Singh & Sinha) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803590
Parmelina nagalandica K. Singh & Sinha (1993: 464); Parmelinopsis nagalandica (K. Singh & Sinha) Divakar &
Upreti (2005: 288).
Hypotrachyna neodamaziana (Elix & J. Johnst.) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov.
MycoBank No.: MB 803591
Parmelina neodamaziana Elix & Johnston (1986: 155); Parmelinopsis neodamaziana (Elix & J. Johnst.) Elix & Hale
(1987: 243).
Hypotrachyna neoprotocetrarica Divakar, A. Crespo, Sipman, Elix & Lumbsch, nom. nov. MycoBank No.:
MB 803592
Parmelinopsis protocetrarica Elix (1993a: 119); non Hypotrachyna protocetrarica Elix, T.H. Nash & Sipman in Sipman
et al. (2009: 127).
Hypotrachyna schindleri (Hale) Divakar, A. Crespo, Sipman, Elix & Lumbsch, comb. nov. MycoBank No.:
MB 803593
Parmelina schindleri Hale (1976: 44); Parmelinopsis schindleri (Hale) Elix & Hale (1987: 243).
Acknowledgements
This work was supported by the Spanish Ministerio de Ciencia e Innovación (CGL2010-21646/BOS) and
Ramón y Cajal grant (RYC02007-01576) to PKD, the Universidad Complutense-Banco Santander (GR 35/
10A), Comunidad Autónoma de Madrid (REMEDINAL S-2009/AMB-1783), the National Science
Foundation (“Hidden diversity in parmelioid lichens”, DEB-0949147), and the Polish National Centre for
Research and Development (LIDER Program, 92/L–1/09). Sequencing was performed in the Centro de
Genómica y Proteómica del Parque Científico de Madrid, where Maria Isabel García Saez is especially
thanked. The authors thank two anonymous reviewers for valuable comments and suggestions and Michel
Benatti and James Lendermer for providing valuable material for our studies.
References
Adler, M. & Elix, J.A. (1987) Three new saxicolous species in Parmeliaceae (lichenized Ascomycotina) from Argentina.
Mycotaxon 30: 339–344.
Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–
723.
http://dx.doi.org/10.1109/tac.1974.1100705
Amo de Paz, G., Lumbsch, H.T., Cubas, P., Elix, J.A. & Crespo, A. (2010a) The genus Karoowia (Parmeliaceae,
Ascomycota) includes unrelated clades nested within Xanthoparmelia. Australian Systematic Botany 23: 173–184.
http://dx.doi.org/10.1071/sb09055
Amo de Paz, G., Lumbsch, H.T., Cubas, P., Elix, J.A. & Crespo, A. (2010b) The morphologically deviating genera
Omphalodiella and Placoparmelia belong to Xanthoparmelia (Parmeliaceae). Bryologist 113: 376–386.
http://dx.doi.org/10.1639/0007-2745-113.2.376
Aptroot, A. (1991) Lichens of Madagascar: new records and species of Parmeliaceae. Cryptogamie, BryologieLichénologie 12: 149–154.
Awasthi, D.D. (1976) Lichen genus Parmelia in India I, Subgenera Parmelia and Amphigymnia. Biological Memoirs 1:
155–266.
34 •
Phytotaxa 132 (1) © 2013 Magnolia Press
DIVAKAR ET AL.
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.
http://dx.doi.org/10.3852/mycologia.97.1.150
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. Mycological Research 108: 873–884.
http://dx.doi.org/10.1017/s0953756204000723
Blanco, O., Crespo, A., Elix, J.A., Hawksworth, D.L. & Lumbsch, H.T. (2004b) A molecular phylogeny and a new
classification of parmelioid lichens containing Xanthoparmelia-type lichenan (Ascomycota: Lecanorales). Taxon 53:
959–975.
Blanco, O., Crespo, A., Ree, R.H. & Lumbsch, H.T. (2006) Major clades of parmeliold lichens (Parmeliaceae,
Ascomycota) and the evolution of their morphological and chemical diversity. Molecular Phylogenetics and
Evolution 39: 52–69.
http://dx.doi.org/10.1016/j.ympev.2006.03.024
Bouly de Lesdain, M. (1933) Lichens du Mexique, recueillis par les frères G. Arsène et Amable Saint-Pierre. III
Supplément. Annales de Cryptogamie Exotique 6: 99–130.
Brusse, F. A. (1991) A new species in the lichen genus Parmelia (Parmeliaceae, Ascomycotina), from the Blouberg,
northern Transvaal, South Africa, with further notes on southern African lichens. Mycotaxon 42: 163–169.
Chen, J.-B., Wu, J.-N. & Wei, J.-C. (1989) Lichens of Shennongjia. In: Fungi and Lichens of Shennongjia, pp. 386-493.
Beijing: World Publishing Corp.
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.
Molecular Biology and Evolution 17: 540–552.
http://dx.doi.org/10.1093/oxfordjournals.molbev.a026334
Crespo, A., Blanco, O. & Hawksworth, D.L. (2001) The potential of mitochondrial DNA for establishing phylogeny and
stabilising generic concepts in the parmelioid lichens. Taxon 50: 807–819.
Crespo, A., Divakar, P.K. & Hawksworth, D.L. (2011) Generic concepts in parmelioid lichens, and the phylogenetic
value of characters used in their circumscription. Lichenologist 43: 511–535.
http://dx.doi.org/10.1017/s0024282911000570
Crespo, A., Ferencova, Z., Pérez-Ortega, S., Argüello, A., Elix, J.A. & Divakar, P.K. (2010a) Austroparmelina, a new
Australasian lineage in parmelioid lichens (Parmeliaceae, Ascomycota): a multigene and morphological approach.
Systematics and Biodiversity 8: 209–221.
Crespo, A., Kauff, F., Divakar, P.K., Amo, G., Arguello, A., Blanco, O., et al. (2010b) Phylogenetic generic classification
of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological and chemical evidence.
Taxon 59: 1735–1753.
Crespo, A., Lumbsch, H.T., Mattsson, J.E., Blanco, O., Divakar, P.K., Articus, K., et al. (2007) Testing morphologybased hypotheses of phylogenetic relationships in Parmeliaceae (Ascomycota) using three ribosomal markers and
the nuclear RPB1 gene. Molecular Phylogenetics and Evolution 44: 812–824.
Culberson, C.F. (1972) Improved conditions and new data for the identification of lichen products by a standardized thinlayer chromatographic method. Journal of Chromatography 72: 113–125.
http://dx.doi.org/10.1016/0021-9673(72)80013-x
Culberson, C.F. & Johnson, A. (1982) Substitution of methyl tert.-butyl ether for diethyl ether in standardized thin-layer
chromatographic method for lichen products. Journal of Chromatography 238: 438–487.
http://dx.doi.org/10.1016/s0021-9673(00)81336-9
Culberson, W.L. & Culberson, C.F. (1981) The genera Cetrariastrum and Concamerella (Parmeliaceae): a
chemosynthetic synopsis. Bryologist 84: 273–314.
http://dx.doi.org/10.2307/3242843
Degelius, G.N. (1941) Contributions to the Lichen flora of North America II. The lichen flora of the Great Smoky
Mountains. Arkiv för Botanik 30A, Nr. 3: 1–80.
DePriest, P.T. & Hale, B.W. (1998) New combinations in parmelioid genera (Ascomycotina: Parmeliaceae). Mycotaxon
67: 201–206.
Divakar, P.K., Blanco, O., Hawksworth, D.L. & Crespo, A. (2005) Molecular phylogenetic studies on the Parmotrema
reticulatum (syn. Rimelia reticulata) complex, including the confirmation of P. pseudoreticulatum as a distinct
species. Lichenologist 37: 55–65.
http://dx.doi.org/10.1017/s0024282904014586
Divakar, P.K., Crespo, A., Blanco, O. & Lumbsch, H.T. (2006) Phylogenetic significance of morphological characters in
the tropical Hypotrachyna clade of parmelioid lichens (Parmeliaceae, Ascomycota). Molecular Phylogenetics and
Evolution 40: 448–458.
http://dx.doi.org/10.1016/j.ympev.2006.03.024
Divakar, P.K., Del Prado, R., Lumbsch, H.T., Wedin, M., Esslinger, T.L., Leavitt, S.D., et al. (2012) Diversification of the
MOLECULAR PERSPECTIVE ON GENERIC CONCEPTS IN HYPOTRACHYNA
Phytotaxa 132 (1) © 2013 Magnolia Press
• 35
newly recognized lichen forming fungal lineage Montanelia (Parmeliaceae, Ascomycota) and its relation to key
geological and climatic events. American Journal of Botany 99: 2014–2026.
http://dx.doi.org/10.3732/ajb.1200258
Divakar, P.K., Ferencova, Z., Del Prado, R., Lumbsch, H.T. & Crespo, A. (2010) Remototrachyna, a new tropical lineage
in hypotrachynoid lichens (Parmeliaceae, Ascomycota): a multigene and morphological approach. American
Journal of Botany 97: 579–590.
http://dx.doi.org/10.3732/ajb.0900140
Divakar, P.K.; Upreti, D.K. & Elix, J.A. (2001) New species and new records in the lichen family Parmeliaceae
(Ascomycotina) from India. Mycotaxon 80: 355–362.
http://dx.doi.org/10.1017/s0024282905015215
Divakar, P.K. & Upreti, D.K. (2005) Parmelioid lichens in India (A revisionary study). Bishen Singh Mahendra Pal
Singh, Dehra Dun p. 488.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids
Research 32: 1792–1797.
http://dx.doi.org/10.1093/nar/gkh340
Elix, J.A. (1993a) New species in the lichen family Parmeliaceae (Ascomycotina) from Australia. Mycotaxon 47: 101–
129.
Elix, J.A. (1993b) Progress in the generic delimitation of Parmelia sensu lato lichens (Ascomycotina: Parmeliaceae) and
a synoptic key to the Parmeliaceae. Bryologist 96: 359–383.
Elix, J.A. (1994) Parmeliaceae. Flora of Australia 55: 1–341.
Elix, J.A. & Hale, M.E. (1987) Canomaculina, Myelochroa, Parmelinella, Parmelinopsis and Parmotremopsis, five new
genera in the Parmeliaceae (lichenized Ascomycotina). Mycotaxon 29: 233–244.
Elix, J.A. & Johnston, J. (1986) New species of Parmelina (lichenised Ascomycotina) from Australia and New Zealand.
Brunonia 9: 155–161.
Elix, J.A., Johnston, J. & Verdon, D. (1986) Canoparmelia, Paraparmelia and Relicinopsis, three new genera in the
Parmeliaceae (lichenized Ascomycotina). Mycotaxon 27: 271–282.
Esslinger, T.L. (1978) A new status for the brown Parmeliae. Mycotaxon 7: 45-54.
Fries, E. (1825) Systema Orbis Vegetabilis. Primas lineas novae constrictionis periclitatur Elias Fries. Pars I. Plantae
homonemeae (Vol. 1). Lund, pp. 1–369.
Gutierrez, G., Blanco, O., Divakar, P.K., Lumbsch, H.T. & Crespo, A. (2007) Patterns of group I intron presence in
nuclear SSU rDNA of the lichen family Parmeliaceae. Journal of Molecular Evolution 64: 81–195.
http://dx.doi.org/10.1007/s00239-005-0313-y
Hale, M.E., Jr (1972) Parmelia jamesii, an unusual species in section Imbricaria (Lichenes) from Australia and New
Zealand. Phytologia 23: 179.
Hale, M.E., Jr (1974a) Bulbothrix, Parmelina, Relicina, and Xanthoparmelia, four new genera in the Parmeliaceae.
Phytologia 28: 479–490.
Hale, M. E., Jr (1974b) Delimitation of the lichen genus Hypotrachyna (Vainio) Hale. Phytologia 28: 340–342.
Hale, M. E., Jr. (1975) A revision of lichen genus Hypotrachyna (Parmeliaceae) in tropical America. Smithsonian
Contributions to Botany 25: 1–73.
http://dx.doi.org/10.5479/si.0081024x.25
Hale, M. E., Jr (1976) A monograph of the lichen genus Parmelina Hale (Parmeliaceae). Smithsonian Contributions to
Botany 33: 1–60.
http://dx.doi.org/10.5479/si.0081024x.33
Hale, M.E., Jr (1984) Flavopunctelia, a new genus in the Parmeliaceae (Ascomycotina). Mycotaxon 20: 681–682.
Hale, M.E., Jr (1986a) Arctoparmelia, a new genus in the Parmeliaceae (Ascomycotina). Mycotaxon 25: 251–254.
Hale, M.E., Jr (1986b) Flavoparmelia, a new genus in the lichen family Parmeliaceae (Ascomycotina). Mycotaxon 25:
603–605.
Hale, M.E., Jr. & Fletcher, A. (1990) Rimelia Hale & Fletcher, a new lichen genus (Ascomycotina: Parmeliaceae).
Bryologist 93: 23–29.
http://dx.doi.org/10.1017/s0024282985000329
Hale, M.E., Jr & Wirth, M. (1971) Notes on Parmelia subgenus Everniiformes with descriptions of six new species.
Phytologia 22: 36–40.
Högnabba, F. (2006) Molecular phylogeny of the genus Stereocaulon (Stereocaulaceae, lichenized ascomycetes).
Mycological Research 110: 1080–1092.
http://dx.doi.org/10.1016/j.mycres.2006.04.013
Hörandl, E. & Stuessy, T.F. (2010) Paraphyletic groups as natural units of biological classification. Taxon 59: 1641–
1653.
Huelsenbeck, J. P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–
755.
36 •
Phytotaxa 132 (1) © 2013 Magnolia Press
DIVAKAR ET AL.
http://dx.doi.org/10.1093/bioinformatics/17.8.754
Jiang, Y.-M. & Wei, J.-C. (1993) A new species of Everniastrum containing diffractaic acid. Lichenologist 25: 57–60.
http://dx.doi.org/10.1017/s0024282993000064
Jiang, Y.M. & Wei, J.C. (1989) A preliminary study on Everniastrum from China. Acta Byrolichenologica Asiatica 1:
43–52.
Kärnefelt, I. (1980) Everniastrum andense sp. nov., a neotropical paramo lichen. Botaniska Notiser 133: 387–394.
Krog, H. (1982) Punctelia, a new lichen genus in the Parmeliaceae. Nordic Journal of Botany 2: 287–292.
http://dx.doi.org/10.1111/j.1756-1051.1982.tb01191.x
Krog, H. & Swinscow, T.D.V. (1981) Parmelia subgenus Amphigymnia (lichens) in East Africa. Bulletin of the British
Museum (Natural History), Botany Series 9: 143–231.
http://dx.doi.org/10.1017/s0024282982000528
Krog, H. & Swinscow, T.D.V. (1987) New species and new combinations in some parmelioid lichen genera, with special
emphasis on East African taxa. Lichenologist 19: 419–431.
http://dx.doi.org/10.1017/s0024282987000392
Kurokawa, S. (1968) Parmelia expallida, a new lichen species from eastern Asia. Bulletin of the National Science
Museum (Tokyo), Series B (Botany) 11: 191–194.
Kurokawa, S. (1991) Rimeliella, a new lichen genus related to Rimelia of the Parmeliaceae. Annals of the Tsukuba
Botanical Garden 10: 1–14.
Kurokawa, S. (1999) A note on pustulate or sorediate species of Cetrariastrum (Parmeliaceae). Journal of Japanese
Botany 74: 251–255.
Lumbsch, H.T., Ahti, T., Altermann, S., Amo, G., Aptroot, A., Arup, U., et al. (2011) One hundred new species of
lichenized fungi: a signature of undiscovered global diversity. Phytotaxa 18: 1–127.
Lumbsch, H.T., Hipp, A.L., Divakar, P.K., Blanco, O. & Crespo, A. (2008) Accelerated evolutionary rates in tropical and
oceanic parmelioid lichens (Ascomycota). BMC Evolutionary Biology 8: 257.
Lumbsch, H.T., Parnmen, S., Rangsiruji, A. & Elix, J.A. (2010) Phenotypic disparity and adaptive radiation in the genus
Cladia (Lecanorales, Ascomycota). Australian Systematic Botany 23: 239–247.
Lutzoni, F., Kauff, F., Cox, C., McLaughlin, D., Celio, G., Dentinger, B., et al. (2004) Assembling the fungal tree of life:
progress, classification, and evolution of subcellular traits. American Journal of Botany 91: 1446–1480.
http://dx.doi.org/10.3732/ajb.91.10.1446
Mackay, J.T. (1836) Flora Hibernica, vol. 2. William Curry, Inn and Co., Dublin. 279 p.
Magnusson, A.H. (1941) New species of Cladonia and Parmelia from the Hawaiian Islands. Arkiv för Botanik 30B(3):
1–9.
Marcano, V., Morales Méndez, A., Sipman, H. & Calderon, L. (1996) A first checklist of the lichen-forming fungi of the
Venezuelan Andes. Tropical Bryology 12: 193–235.
Massalongo, A. (1860) Esame comparativo di alcuni generi di licheni. Atti dell'Istituto Veneto di scienze, lettere ed arti 5,
ser. 3: 247–267, 313–337.
Meyen, J. & Flotow, J. (1843) Lichenes Exotici (Observationes in itinere circum terram institutae (1830-1832):
Lichenes. Nova Acta Academiae Caesariae Leopoldinae-Carolinae 19, Suppl.: 209–232.
Nylander, J.A.A., Wilgenbusch, J.C., Warren, D.L. & Swofford, D.L. (2007) AWTY (Are We There Yet?): a system for
graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24: 581–583.
http://dx.doi.org/10.1093/bioinformatics/btm388
Page, R.D.M. (1996) Treeview: an application to display phylogenetic trees on personal computers. Computer Applied
Biosciences 12: 357–358.
http://dx.doi.org/10.1093/bioinformatics/12.4.357
Parnmen, S., Rangsiruji, A., Mongkolsuk, P., Boonpragob, K., Elix, J. A. & Lumbsch, H.T. (2010) Morphological
disparity in Cladoniaceae: The foliose genus Heterodea evolved from fruticose Cladia species (Lecanorales,
lichenized Ascomycota). Taxon 59: 841–849.
Pooprang, T., Boonpragob, K. & Elix, J.A. (1999) New species and new records in the lichen family Parmeliaceae
(Ascomycotina) from Thailand. Mycotaxon 71: 111–127.
Posada, D. (2008) JModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.
http://dx.doi.org/10.1093/molbev/msn083
Santesson, R. (1942) Two interesting new species of the lichen genus Parmelia. Botaniska Notiser 1942: 325–330.
Schmidt, H.A., Strimmer, K., Vingron, M. & von Haeseler, A. (2002) TREE-PUZZLE: maximum likelihood
phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.
http://dx.doi.org/10.1093/bioinformatics/18.3.502
Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic
inference. Molecular Biology and Evolution 16: 1114–1116.
http://dx.doi.org/10.1093/oxfordjournals.molbev.a026201
Singh, K.P. & Sinha, G.P. (1993) Two new species of Parmelina from India. Nordic Journal of Botany 13: 463–466.
MOLECULAR PERSPECTIVE ON GENERIC CONCEPTS IN HYPOTRACHYNA
Phytotaxa 132 (1) © 2013 Magnolia Press
• 37
http://dx.doi.org/10.1111/j.1756-1051.1993.tb00082.x
Sipman, H.J.M. (1980) Studies on Colombian cryptogams. X. The genus Everniastrum Hale and related taxa (Lichens).
Proceedings Koninkijke Nederlandse Akademie van Wetenschappen, ser. C 83: 333–354.
Sipman, H. J. M. (1986) Notes on the lichen genus Everniastrum (Parmeliaceae). Mycotaxon 26: 235–251.
Sipman, H.J.M., Elix, J.A. & Nash, T.H. (2009) Hypotrachyna (Parmeliaceae, Lichenized Fungi). Flora Neotropica
Monograph 104: 1–176.
Smith, J.E. & Sowerby, J. (1809) English Botany, vol. 29. White, London.
Smith, C. W. (1993) Notes on Hawaiian parmelioid lichens. Bryologist 96: 326–332.
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and
mixed models. Bioinformatics 22: 2688–2690.
http://dx.doi.org/10.1093/bioinformatics/btl446
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML Web Servers. Systematic
Biology 57: 758–771.
http://dx.doi.org/10.1080/10635150802429642
Stenroos, S.K. & DePriest, P.T. (1998) SSU rDNA phylogeny of cladoniiform lichens. American Journal of Botany 85:
1548–1559.
http://dx.doi.org/10.2307/2446481
Strimmer, K. & Rambaut, A. (2002) Inferring confidence sets of possibly misspecified gene trees. Proceedings of the
Royal Society of London, Ser. B, Biological Sciences 269: 137–142.
http://dx.doi.org/10.1098/rspb.2001.1862
Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned
blocks from protein sequence alignments. Systematic Biology 56: 564–577.
http://dx.doi.org/10.1080/10635150701472164
Taylor, T. (1847) New lichens, principally from the herbarium of Sir William J. Hooker. Journal of Botany 6: 148–197.
Tehler, A. & Irestedt, M. (2007) Parallel evolution of lichen growth forms in the family Roccellaceae (Arthoniales,
Ascomycota). Cladistics 23: 432–454.
Thell, A., Feuerer, T., Elix, J.A. & Kärnefelt, I. (2006) A contribution to the phylogeny and taxonomy of Xanthoparmelia
(Ascomycota, Parmeliaceae). Journal of the Hattori Botanical Laboratory 100: 797–807.
Thell, A., Crespo, A., Divakar, P.K., Kärnefelt, I., Leavitt, S.D., Lumbsch, H.T., et al. (2012) A review of the lichen
family Parmeliaceae - history, phylogeny and current taxonomy. Nordic Journal of Botany 30: 641–664.
http://dx.doi.org/10.1111/j.1756-1051.2012.00008.x
Vainio, E.A. (1899) Lichenes novi rarioresque. Hedwigia 38, Beibl. 3: (121) – (125).
Wei, J.C. & Jiang, Y.M. (1982) New materials for lichen flora of Xizang. Acta Phytotaxonomica Sinica 20: 496–501.
Wirtz, N., Printzen, C., Sancho, L.G. & Lumbsch, H.T. (2006) The phylogeny and classification of Neuropogon and
Usnea (Parmeliaceae, Ascomycota) revisited. Taxon 55: 367–376.
Zahlbruckner, A. (1909) Lichenes (Flechten). In: Ergebnisse der botanischen Expedition der kaiserlichen Akademie der
Wissenschaften nach Südbrasilien. Denkschriften der Kaiserlichen Akademie der Wissenschaften 83: 85–211.
http://dx.doi.org/10.1007/978-3-7091-5790-9
Zahlbruckner, A. (1929) Catalogus Lichenum Universalis (Vol. 6). Leipzig: Borntraeger.
38 •
Phytotaxa 132 (1) © 2013 Magnolia Press
DIVAKAR ET AL.