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1
American Journal of Botany 100(5): 000–000. 2013.
American Journal of Botany 100(5): 1–13, 2013 ; http://www.amjbot.org/ © 2013 Botanical Society of America
Lichens represent one of the most successful biological life-
styles known, being able to colonize a wide range of substrata
in almost all terrestrial ecosystems and often under conditions
where little or no plant growth is possible, such as hot and cold
deserts ( Friedmann and Galun, 1974 ; Kappen, 1982 , 1988 ;
Kershaw, 1985 ; Ahmadjian, 1993 ; Eldridge, 1997 ; Brodo et al.,
2001 ; Øvstedal and Smith, 2001 ; Pereira et al., 2007 ; Nash,
2008 ). Most organisms, including vascular plants, have their
highest biodiversity in tropical latitudes, where they often also
produce their highest biomass ( Rohde, 1992 ; Blackburn and
Gaston, 1997 ; Brown and Lomolino, 1998 ; Gaston, 2000 ; Bokma
and Monkkonen, 2001 ; Koleff and Gaston, 2001 ; Willig et al.,
2003 ; Hillebrand, 2004 ; Currie et al., 2004 ). Lichenized fungi
were long believed to be an exception to this rule ( Lücking et al.,
2009b ). However, recent studies have shown that tropical low-
land rainforest harbor the highest species richness and tropical
montane rainforests and páramos produce lichen biomass com-
parable to lichen-rich boreal regions ( Aptroot and Sipman, 1997 ;
Lücking et al., 2009b ). Lichen biodiversity hotspots are also
found in subtropical deserts, particularly the Sonoran, Atacama,
and Namib deserts ( Redón, 1982 ; Nash et al., 2002 , 2004 , 2007 ;
Mittermeier et al., 2005 ; Wirth, 2010 ).
The origin of lichenization is disputed ( Retallack, 1994 ,
1995 , 2007 ; Gargas et al., 1995 ; Lutzoni et al., 2001 ; Tehler et al.,
2003 ; Eriksson, 2005 ; Hawksworth, 2005 ; Lücking et al., 2009a ;
Nelsen et al., 2009 , 2011 ; Schoch et al., 2009 ). The immediate
sister group of the Dikaryomycota, the Glomeromycota, is en-
tirely mutualistic, and fossils believed to be lichens go back as
far as 400 to 600 million years ago (Ma) ( Taylor et al., 1997 ;
Yuan et al., 2005 ), so primitive lichen-like associations could
have existed early on in the evolution of Fungi and given rise
1 Manuscript received 17 October 2012; revision accepted 26 February
2013.
This study was supported by a grant from the National Science
Foundation: ATM—Assembling a taxonomic monograph: The lichen
family Graphidaceae (DEB-1025861 to The Field Museum: T. Lumbsch
[PI], R. Lücking [CoPI]). Herbarium curators Othmar Breuss (W), Bruno
Dennetiére (PC), Peter Mansfeld (KASSEL), and Michaela Schmull (FH)
are thanked for their collaboration. We are grateful to Martin Irestedt
who swiftly provided laboratory assistance at Molekylärsystematiska
Laboratoriet, Naturhistoriska riksmuseet. The Galapagos Lichen Inventory
is possible because of the long-term support by the Galapagos National
Park, especially its technical director Washington Tapia. The Galapagos
aspect of this study has received fi nancial support by the Erwin Warth
Stiftung and the Bay and Paul Foundations. This publication is contribution
number 2057 of the Charles Darwin Foundation for the Galapagos
Islands.
6 Author for correspondence (e-mail: rlucking@fi eldmuseum.org)
doi:10.3732/ajb.1200548
J OURNEY FROM THE WEST: DID TROPICAL GRAPHIDACEAE
(LICHENIZED ASCOMYCOTA: OSTROPALES) EVOLVE FROM
A SAXICOLOUS ANCESTOR ALONG THE AMERICAN PACIFIC COAST? 1
R OBERT L ÜCKING 2,6 , A NDERS T EHLER 3 , F RANK B UNGARTZ 4 , E IMY R IVAS PLATA 2,5
AND H. THORSTEN L UMBSCH 2
2 Department of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, Illinois 60605 USA;
3 Naturhistoriska
Riksmuseet, Enheten för Kryptogambotanik, Box 50007 104 05 Stockholm, Sweden;
4 Fundación Charles Darwin, Casilla
200144, Isla Santa Cruz, Galapagos, Ecuador; and
5 Department of Biology, Duke University, 125 Science Drive, Durham, North
Carolina 27708, USA
• Premise of the study: This study elucidates the phylogenetic position of a unique taxon of Graphidaceae occurring on rock in
coastal desert areas, assessing its importance for our understanding of the evolution of the largest family of tropical lichenized
fungi.
• Methods: We used maximum likelihood and Bayesian approaches to reconstruct a three-gene phylogeny of Graphidaceae and
a Bayesian molecular clock approach to estimate divergence dates for major clades, as well as Bayesian ancestral ecogeogra-
phy state analysis.
• Key results: The new genus Redonographa represents a new subfamily, Redonographoideae, sister to subfamily Graphidoideae.
Redonographa is exclusively saxicolous and restricted to the American Pacifi c coast from California to central Chile, including
Galapagos. It contains four species: Redonographa chilensis comb. nov., R. saxiseda comb. nov., R. saxorum comb. nov., and
R. galapagoensis sp. nov. The genus Gymnographopsis , with a similar ecogeography but differing in excipular carbonization
and chemistry, is also included in Redonographoideae, with the species G. chilena from Chile and G. latispora from South
Africa. Molecular clock analysis indicates that Redonographoideae diverged from Graphidoideae about 132 million years ago
(Ma) in the Early Cretaceous.
• Conclusions: The divergence date for subfamilies Redonographoideae and Graphidoideae coincides with the early breakup of
Gondwana and ancient origin of the Atacama Desert. However, the common ancestor of Redonographoideae plus Graphi-
doideae was reconstructed to be tropical-epiphytic. Thus, even if Redonographoideae is subtropical-saxicolous, the hypothesis
that Graphidoideae evolved from a subtropical-saxicolous ancestor is not supported.
Key words: Graphidaceae; lichens; Mediterranean regions; Ostropales; Pacifi c Desert; rock-inhabiting; Sonoran Desert.
http://www.amjbot.org/cgi/doi/10.3732/ajb.1200548The latest version is at
AJB Advance Article published on April 17, 2013, as 10.3732/ajb.1200548.
Copyright 2013 by the Botanical Society of America
2AMERICAN JOURNAL OF BOTANY [Vol. 100
morphology and chemistry as C. chilensis , known from Chile
( C. saxiseda ) and California, Baja California, and the Galapa-
gos Islands ( C. saxorum ; Bungartz et al., 2010 ; Lücking, 2013 ;
see below). In an attempt to confi rm the systematic position of
these species within Graphidaceae, we obtained parts of the
mitochondrial small subunit (mtSSU), nuclear large subunit
ribosomal RNA gene (nuLSU), and the second largest RNA
polymerase subunit ( RPB2 ) genes for three samples of Carba-
canthographis chilensis and one sample of C. saxiseda and
performed a phylogenetic analysis in the framework of two
phylum- and family-wide data sets ( Rivas Plata et al., 2013 ).
Much to our surprise, the sequenced species represent a novel
lineage within Graphidaceae, being sister to subfamily Graphi-
doideae, which contains the bulk of species in Graphidaceae
( Rivas Plata et al., 2012 ). The peculiar ecology and distribution
of these lichens, with a distribution in the Sonoran, Pacifi c Desert,
and Galapagos biogeographical provinces ( Udvardy, 1975 ),
provided a framework to assess the early evolution of Graphi-
daceae and specifi cally subfamily Graphidoideae, which, similar
to other lichenized lineages, could have evolved from a saxi-
colous ancestor characteristic of subtropical, warm climates. A
molecular clock analysis is provided to place the evolution of
these lineages within Graphidaceae into a palaeoclimatic and
palaeoecological context.
MATERIALS AND METHODS
Specimen sampling and taxonomy — New species sampled for DNA se-
quencing were Carbacanthographis chilensis and C. saxiseda from the Co-
quimbo and Atacama provinces in Chile (Appendix S1, see Supplemental Data
with the online version of this article): Chile. Coquimbo: Tongoy, on the hill
above town; 30 ° 15 ′ S, 71 ° 31 ′ W, 80 m a.s.l.; November 2001, Tehler 8370
(S-L28647); 30 km N of La Serena, 2 km S Los Hornos, on slope toward ocean;
29 ° 39 ′ S, 71 ° 18 ′ W, 80 m a.s.l.; November 2001, Tehler 8407 (S-L28675); Punta
Teatinos just N of La Serena; 29 ° 49 ′ S, 71 ° 17 ′ W; October 2009, Tehler 9887
(S-F206087). Antofagasta: Cerro Moreno a few km W Juan Lopez N of Antofa-
gasta, on the southern slope of the mountain; 23 ° 31 ′ S, 70 ° 34 ′ W, 150–900 m
a.s.l.; October 2009, Tehler 9927 (S-F206110). These and other herbarium
specimens including types were studied at F and S and at the herbaria of FH and
PC, using standard methods of light microscopy and thin-layer chromatography
( Orange et al., 2001 ; Lumbsch, 2002 ).
DNA extraction and molecular methods — We generated new DNA se-
quences from three loci (mtSSU, nuLSU, RPB2 ). Extractions, amplifi cations,
and sequencing followed the procedures of Tehler and Irestedt (2007) and
Tehler et al. (2009a , b ). Primers for amplifi cation were (a) for nuLSU: LROR
and LR5 ( Vilgalys and Hester, 1990 ), (b) for mtSSU: mr-SSU1 and Mr-SSU3R
( Zoller et al., 1999 ), and (c) for RPB2 : fRPB2-7cF and fRPB2-11aR ( Liu et al.,
1999 ). The sequence fragments were assembled to complete sequences with
the program SeqMan II(tm) (DNASTAR, Madison, Wisconsin, USA). Am-
biguous nucleotide positions were coded with the appropriate IUPAC codes.
All new sequences were submitted to GenBank (online Appendix S1).
Phylogenetic analyses — The newly generated sequences were analyzed
both separately and combined within a larger data set of Ascomycota (including
subfamily Gomphilloideae) and a data set focusing on Graphidaceae (excluding
subfamily Gomphilloideae). For the Ascomycota data set, we used the same
taxa and alignments as E. Rivas Plata et al. (unpublished manuscript ) did, and
for the Graphidaceae data set, we used a subset of the data analyzed by Rivas
Plata et al. (2013) with one species per genus or genus-level clade selected
(online Appendix S1). Sequences were arranged into multiple sequence align-
ments (MSA) for each gene using the program BIOEDIT 7.09 ( Hall, 1999 ) and
automatically aligned with MAFFT using the auto option ( Katoh and Toh,
2005 ). The unaligned MSA for the mtSSU and the nuLSU gene partitions
was also submitted to the GUIDANCE web server at http://guidance.tau.ac.il
to assess alignment confi dence scores for each site ( Penn et al., 2010a , b ).
GUIDANCE uses a MAFFT alignment and returns a colored MSA that allows
to nonlichenized fungal lineages ( Tehler et al., 2003 ; Eriksson,
2005 ). However, for extant lichenized lineages such as Artho-
niomycetes, Lecanoromycetes, Lichinomycetes, Eremithallales,
Trypetheliales, and Verrucariales in Ascomycota and Dicty-
onema , Lepidostroma , Lichenomphalia , Marchandomphalina ,
and Multiclavula in Basidiomycota, evidence points to a more
recent, multiple origin of these from nonlichenized ancestors
between 300 and 200 Ma ( Gargas et al., 1995 ; Lawrey et al.,
2009 ; Nelsen et al., 2009 , 2011 ; Schoch et al., 2009 ). In the
absence of a good fossil record, molecular clock dating studies
indicate that most lichenized lineages, at least in the Ascomy-
cota, evolved in the relatively dry, warm Triassic, during which
extended terrestrial forest vegetation was sparsely developed
( Amo de Paz et al., 2011 ; E. Rivas Plata et al., unpublished
manuscript ). This hypothesis is consistent with the fi nding that
in several cases, saxicolous lichens or even nonlichenized
rock fungi are basal or sister to the main lichenized lineages
( Miadlikowska et al., 2006 ; Hofstetter et al., 2007 ; Gueidan
et al., 2008 ; Schoch et al., 2009 ). In many lichenized lineages,
however, the immediate sister group is not known, which makes
assumptions about their early evolution speculative.
Graphidaceae is presumably the largest family of lichenized
fungi, with nearly 2000 species known and probably several
hundred more yet to be discovered ( Staiger 2002 ; Frisch et al.,
2006 ; Kirk et al., 2008 ; Rivas Plata and Lücking 2013 ; Rivas
Plata et al., 2012 , 2013 ; Sipman et al., 2012 ). The family is es-
sentially tropical, with the highest diversity found in tropical
lowland to montane rain forest and only a few species extend-
ing into extratropical regions ( Wirth and Hale, 1963 , 1978 ; Hale
1974 , 1978 , 1981 ; Rivas Plata et al., 2008 ; Sipman et al., 2012 ).
While the family is predominantly epiphytic, a few lineages
deviate by their unique ecology, particularly the genus Diplo-
schistes , which is mainly found in subtropical and tropical mon-
tane regions on exposed soil and rock substrata and also has a
photobiont different from most other Graphidaceae ( Lumbsch,
1989 ; Guderley and Lumbsch, 1996 ; Lumbsch, 2002 ; Lumbsch
and Elix, 2003 ). With the data available, ancestral character
state analysis indicates a tropical-epiphytic ancestor for Graphi-
daceae, with lineages such as Diploschistes being derived ( Rivas
Plata and Lumbsch, 2011 ). Thus far, it has been diffi cult to test
this hypothesis further, since Diploschistes evolved on a very
long stem branch and its closest living relative remains un-
known ( Martín et al., 2003 ; Fernández-Brime et al., 2011 ; Rivas
Plata et al., 2013 ). Also, no other predominantly or exclusively
nontropical, nonepiphytic lineage was known in the family ex-
cept for the monospecifi c genera Anomalographis , Gymnographa ,
Gymnographopsis , and Sarcographina ( Staiger, 2002 ; Archer,
2009 ). However, these have not yet been sequenced, and their
phylogenetic affi nities are uncertain.
The lichen fungus described as Medusulina chilena and sub-
sequently known as Minksia chilensis ( Dodge, 1966 ; Huneck
and Follmann, 1967 ; Redón and Follmann, 1972 ) is a saxicolous
species from the Chilean Pacifi c desert region (Atacama Desert)
that had been referred to Arthoniales ( Redón and Follmann,
1972 ). Coincidentally, it had also been described in the genus
Opegrapha , as O. petraea , 114 yr before its “rediscovery” ( Montagne,
1852 ; Nylander 1855 ), a name later replaced with Graphis chil-
ensis ( Zahlbruckner, 1923 ). Morphological and anatomical
studies indicated that this species belongs in Graphidaceae,
where it was found to be most similar to Carbacanthographis
and was recombined into that genus ( Lücking, 2013 ). The species
appears to have two close relatives in Carbacanthographis
saxiseda and C. saxorum , saxicolous species with the same
3
May 2013] LÜCKING ET AL.—EVOLUTION OF GRAPHIDACEAE
sister to Fissurinoideae ( Fig. 2 ; online Appendices S8–S9). This
lineage is not congeneric with any of the currently recognized
genera in Graphidaceae, and hence the genus Redonographa is
formally introduced next. Two alternative solutions are possible
based on this topology: either including Redonographa as most
basal lineage within subfamily Graphidoideae, or establishing a
new subfamily for it. Since the branch leading to subfamily
Graphidoideae is rather long and supported, while the backbone
within the latter is shallow and unsupported, we prefer the sec-
ond alternative and therefore formally introduce the new sub-
family Redonographoideae below.
Redonographa Lücking, Tehler & Lumbsch, gen. nov —
[Mycobank MB 803247]. Differing from Carbacanthographis
in the exclusively saxicolous growth habit and the predomi-
nantly smooth periphysoids. Thallus rather thick, continuous to
areolate, ecorticate or with compacted pseudocortex. Lirellae
erumpent to prominent, unbranched to stellately branched or
appearing in pseudostromatic clusters, with basal to almost
complete thalline margin. Excipulum completely carbonized in
mature lirellae, overarching over the hymenium and with short,
smooth or apically warty periphysoids above the hymenium.
Hymenium clear. Ascospores 8 per ascus, ellipsoid to oblong,
transversely 3–5-septate or submuriform with 3–5 transverse
and 0–2 longitudinal septa per segment, with thickened septa
and lens-shaped to rounded lumina, hyaline, with negative Io-
dine (Lugol) reaction. Secondary chemistry: norstictic acid.
The genus is named in honor of Prof. Dr. Jorge Redón
Figueroa, for his contributions to Chilean lichenology ( Redón,
1973 , 1974 , 1982 ; Redón and Lange, 1983 ). Jorge Redón Figueroa
is a Botany Professor at the Universidad Viña del Mar, Prof.
Emeritus at the Universidad de Chile (Facultad de Ciencias) and
the Universidad de Valparaíso (Instituto de Oceanología) and
obtained his doctorate in natural sciences from the Universität
Würzburg in Germany; he has worked on lichens from Chile
and Antarctica.
Type: Redonographa chilensis (Zahlbr.) Lücking & Tehler.
Redonographoideae Lücking, Tehler & Lumbsch, subfam.
nov — [Mycobank MB 803248]. Differing from subfamilies
Fissurinoideae and Graphidoideae in the exclusively saxicolous
growth in subtropical coastal fog deserts and dry coastal habi-
tats, as well as in the following nuLSU DNA sequence patterns,
which cause the nuLSU sequences to blast with Teloschistales
and Lecanorales, rather than Graphidaceae (even if supported
within Graphidaceae in phylogenetic analysis): position 110–112:
CCG vs. TGT; position 315: A vs. (CT); and position 546–548:
delimiting ambiguously aligned portions of the MSA. These were then ex-
cluded from further analysis. This resulted in alignments of 708/995 sites for
the mtSSU, 1343/972 sites for the nuLSU, and 2142/951 for RPB2 , for a total
of 4193/2918 sites in the combined Ascomycota/Graphidaceae data sets. Each
gene was analyzed separately and, after testing for supported topological con-
fl icts ( Mason-Gamer and Kellogg, 1996 ; Miadlikowska and Lutzoni, 2000 ;
Kauff and Lutzoni, 2002 ), the three genes were combined into a single super-
matrix for the Graphidaceae data set. Individual data sets and the combined
supermatrix were subjected to maximum likelihood search using the program
RAxML-HPC BlackBox 7.3.2 on the Cipres Gateway server ( Stamatakis, 2006 ;
Stamatakis et al., 2005 , 2008 ; Miller et al., 2010 ; http://www.phylo.org/portal2/
login!input.action), with parametric bootstrapping generating 350 replicates as
automatically determined by RAxML using a saturation criterion. The univer-
sal GTR-Gamma model was chosen for the analysis. Resampling tree searches
were also done with parsimony jackknifi ng ( Farris et al., 1996 ) as implemented
in the program TNT ( Goloboff et al., 2008 ) using sectorial search, ratcheting,
drifting, tree fusing, and driven search options in effect, all with default set-
tings. For this, 1000 replicates submitted to tree-bisection-reconnection (TBR)
branch swapping were conducted.
Ancestral ecogeographical character state reconstruction analysis — An-
cestral ecogeographical character state reconstruction analysis was performed
using a stochastic Bayesian approach to character mapping ( Huelsenbeck et al.,
2003 ) implemented in SIMMAP 1.5 ( Bollback, 2006 ), as was done previously
in biogeographical studies ( Lopez-Vaamonde et al., 2009 ; Amo de Paz et al.,
2011 ). We treated the major ecogeographic regions as discrete characters,
which were categorized broadly into three traits as multistate characters: wet
tropical (0), wet extratropical (1), and semiarid to arid subtropical or “mediter-
ranean” (2). The best-scoring maximum likelihood tree computed in RAxML
was used as reference tree and terminals were coded as wet tropical (0), with the
exception of Melanotopelia , Schizotrema , and Topeliopsis as wet extratropical
(1), and Diploschistes and Redonographa as “mediterranean” (2).
Molecular clock analysis — A relaxed, uncorrelated lognormal molecular
clock model was employed to date the evolutionary origin of stem and crown
nodes of major lineages of Graphidaceae. The program BEAST 1.6.1 ( Drum-
mond and Rambaut, 2007 ) was used for this purpose, with the following speci-
fi cations: GTR substitution model with base frequencies estimated and Gamma
and invariant sites with six Gamma categories, speciation through a Yule pro-
cess as tree prior, and other priors and operators set to default values. We used
the results from E. Rivas Plata et al. (unpublished manuscript ), calibrated with
several fossils and with similar node age estimates as Berbee and Taylor (2010)
in an independent study using a cross-kingdom approach, as external calibra-
tion, with the Graphidaceae stem node set to 178 ± 18 Ma and the crown node
set to 156 ± 16 Ma.
RESULTS
Phylogeny and systematics — Separate analysis of each gene
(mtSSU, nuLSU, RPB2 ) within a wide taxon sampling of se-
lected Ascomycota confi rmed placement of the analyzed se-
quences with Graphidaceae (supported), being sister to Graphi-
doideae for the mtSSU gene (supported) and the nuLSU gene
(unsupported), and occupying a nested position within Graphi-
doideae for the RPB2 gene (unsupported; Fig. 1 ; for com-
plete trees see Appendices S2–S4 with online Supplemental
Data). Similarly, separate analysis of each gene within the
Graphidaceae data set placed the analyzed sequences sister
to Graphidoideae (mtSSU, supported), sister to Fissurinoideae
plus Graphidoideae (nuLSU, unsupported), and together with
Fissurinoideae nested within Graphidoideae ( Fig. 1 ; for com-
plete trees see online Appendices S5–S7). The combined analy-
sis of the three-gene supermatrix focusing on Graphidaceae,
with Gyalectales as outgroup, placed the target lineage as sister
to Graphidoideae with good support under a maximum likeli-
hood (82%) and a maximum parsimony framework (81%) and
with strong support (1.00) under a Bayesian framework, and the
combined lineage with strong support (98%, 100%, 1.00) as
Fig. 1. Alternative topologies for Graphidaceae subfamilies in the in-
dividual gene trees using a broad Ascomycota data set and a data set focus-
ing on Graphidaceae. For complete trees, see online Appendices S2–S7.
4AMERICAN JOURNAL OF BOTANY [Vol. 100
Fig. 2. Bayesian molecular clock tree of the three-gene data set focusing on Graphidaceae, obtained with BEAST. The topology is similar to the maxi-
mum likelihood (ML) tree obtained with RAxML and the Bayesian majority rule consensus tree obtained with MrBAYES (online Appendices S8–S9).
Bootstrap support values from the ML analysis, posterior probabilities from the Bayesian analysis, and jackknife support values from the parsimony analy-
sis are given for the major branches. Scale axis indicates node age estimate in Myr.
5
May 2013] LÜCKING ET AL.—EVOLUTION OF GRAPHIDACEAE
long, 0.3–0.4 mm broad; labia thick, entire, black, along the rim
often with pruina formed by layer of periphysoids; disc con-
cealed; excipulum laterally carbonized, carbonization no ex-
tending below the hymenium; hymenium hyaline, clear (not
inspersed), I– (rarely faintly bluish laterally along the excipu-
lum), 100–120 µm high; ascospores 8 per ascus, ellipsoid to
citriform with narrowed ends, 18–22 × 9–11 µm, submuriform
with 4–5 transverse septa and 1–2 longitudinal septa per seg-
ment, with thickened septa and irregular, often diamond-shaped
(astrothelioid) lumina, hyaline, I–. Chemistry: norstictic acid,
thallus K+ yellow turning red (forming needle shaped crystals
under the microscope). Habitat: growing saxicolous along the
coast underneath wind- and rain-sheltered, shaded overhangs.
Notes: This species is similar to Redonographa chilensis but dif-
fers in the basally uncarbonized excipulum, the irregularly branched
(not stellate or pseudostromatic) ascomata, and the ascospores
with irregular (astrothelioid) lumina. The species is thus far only
known from the Pacifi c coastal desert in Chile. See Fig. 4A–E .
Redonographa saxorum (Egea & Torrente) Lücking &
Tehler, comb. nov. — [Mycobank MB 803252]; Graphis saxorum
Egea & Torrente, Bryologist 100: 207 (1997); Carbacanthogra-
phis saxorum (Egea & Torrente) Lücking & Bungartz in Bungartz
et al., Nova Hedwigia 90: 7 (2010). Type: Mexico, Egea s.n.
(ASU, holotype, not seen). For a detailed description, see Egea
and Torrente (1997) , Staiger and Kalb (2004) , and Bungartz et al.
(2010) . See Fig. 4F .
Second genus: Gymnographopsis C. W. Dodge.
Gymnographopsis chilena C. W. Dodge , Nova Hedwigia 12:
320 (1966); Gymnographopsis chilensis (C. W. Dodge) Follm .,
Nova Hedwigia 14: 227 (1968) [nom. illeg.]. Type: Chile, Foll-
mann 14661 (FH, holotype!). For a detailed description, see
Staiger (2002) . See Fig. 4G–I.
Gymnographopsis latispora Egea & Torrente , Crypt. Bryol.
Lichénol. 17: 308 (1996). Type: South Africa, Egea s.n. (PRE,
holotype, not seen). For a detailed description, see Egea and
Torrente (1996) .
Key to the known species of Gymnographopsis and Re-
donographa— The six known species of Gymnographopsis and
Redonographa can be distinguished using the following key:
1a Excipulum uncarbonized; secondary substances absent or unknown
but thallus not K+ yellow forming red, needle-shaped crystals in mi-
croscopic section ( Gymnographopsis ) 2
1b Excipulum carbonized; norstictic acid present, thallus K+ yellow form-
ing red, needle-shaped crystals in microscopic section ( Redonographa ) 3
2a Ascospores (20–)25–30(–40) × 12–18 µm; no substances detected by
TLC; South Africa Gymnographopsis latispora
2b Ascospores 20–25 × 10–12 µm; with an unknown substance with R
f
values 36-39-16 in A-B ′ -C; northern Chile Gymnographopsis chilena
3a Ascospores transversely 5–7-septate (20–25 × 8–10 µm); lirellae
immersed-erumpent, mostly covered by thallus layer, unbranched to
sparsely branched; California and Baja California, Galapagos Islands
Redonographa saxorum
3b Ascospores (sub)muriform; lirellae erumpent to sessile, with the black
labia mostly exposed, unbranched or stellately branched 4
4a Ascospores submuriform, narrow (15–20 × 4–6 µm); periphysoids
verrucose; ascomata prominent, often partially open; Galapagos
Redonographa galapagoensis
4b Ascospores muriform, broader (15–30 × 8–18 µm); periphysoids
smooth; ascomata erumpent, closed; central to northern Chile 5
CGT vs. (CT)(CT)G. Morphological, anatomical, and chemical
characters otherwise as in Redonographa .
Type: Redonographa Lücking & Tehler.
Redonographa chilensis (Zahlbr.) Lücking & Tehler, comb.
nov — [Mycobank MB 803249]; Graphis chilensis Zahlbr.,
Catal. Lich. Univers. 2: 297 (1923); Carbacanthographis chil-
ensis (Zahlbr.) Lücking, Lichenologist 45: 128 (2013); Ope-
grapha petraea Mont. in Gay, Hist. Fis. Politic. Chile, Bot.: 182
(1852) [non O. petraea Ach., Lich. Univ.: 674 (1810), nec O.
petraea Mont. in Durieu, Fl. D’Algérie, Cryptog. 1: 278 (1846)];
Graphis petraea (Mont.) Nyl., Ann. Sci. Nat., Bot., Sér. 4 3:
186 (1855) [non G. petraea (Ach.) Wallr., Fl. Crypt. Germ. 1: 336
(1831)]. Type: Chile, Gay s.n. (PC, holotype!). = Medusulina
chilena C. W. Dodge, Nova Hedwigia 12: 322 (1966); Minksia
chilena [as ‘ chilensis ’] (C. W. Dodge) Redón & Follmann, Philip-
pia 1: 133 (1972). Type: Chile, Follmann 14458-D (FH, holotype!).
See Fig. 3B–G . For a detailed description, see Lücking (2013) .
Redonographa galapagoensis Bungartz & Lücking, spec.
nov — [Mycobank MB 803250] Type: ECUADOR. Galapagos:
Santiago Island, ca. 5 km inland from the E-coast; 0 ° 16 ′ S,
90 ° 37 ′ W; Bungartz 5208 (CDS 29421, holotype). Diagnosis:
Differing from R. chilensis in the mostly unbranched, promi-
nent, partly open ascomata, verrucose periphysoids, and nar-
rower ascospores. Description: Thallus areolate, whitish gray,
becoming yellowish white in the herbarium; surface smooth,
epruinose. Apothecia prominent, rounded to shortly lirellate;
lirellae broad and short, thickened, unbranched or rarely
sparsely branched, 0.5–1.5 mm long, 0.4–0.8 mm broad; labia
thick, entire, black, basally with thalline margin, apically and
along the rim with distinct pruina formed by layer of per-
iphysoids; disc usually concealed but expanding with age; ex-
cipulum completely carbonized, carbonization extending below
the hymenium; hymenium hyaline, clear (not inspersed), I–
(rarely faintly bluish laterally along the excipulum), 90–120 μ m
high; ascospores 8 per ascus, ellipsoid to oblong, 15–17(–20) ×
4–5 μ m, submuriform with 5–6 transverse septa and 1–2 longi-
tudinal septa per segment, with thickened septa and lens-shaped
to rounded lumina, hyaline, I–. Chemistry: norstictic acid, thal-
lus K+ yellow turning red (forming needle-shaped crystals un-
der the microscope). Habitat: Growing saxicolous along the
coast underneath wind- and rain-sheltered, shaded overhangs.
Notes: This new species is recognized by its rather prominent,
partially open ascomata, the verrucose periphysoids, and the
rather narrow ascospores. The verrucose surface of the per-
iphysoids is different in appearance from the spinulose sur-
face found in Carbacanthographis ( Staiger, 2002 ), a fact that
supports our conclusion that the two genera are not closely
related and do not have shared synapomorphies. Redonographa
galapagoensis appears to be endemic to the Galapagos Islands;
it was previously reported as Carbacanthographis saxiseda
( Bungartz et al., 2010 ) but was found to represent an unde-
scribed taxon. See Fig. 3I–L .
Redonographa saxiseda (Zahlbr.) Lücking & Tehler, comb.
nov — [Mycobank MB 803251]; Graphina saxiseda Zahlbr.,
Acta Horti Gothob. 2: 4 (1925); Carbacanthographis saxiseda
(Zahlbr.) Bungartz in Bungartz et al., Nova Hedwigia 90: 6
(2010). Type: Chile, Skottsberg s.n. (W, holotype!). Description:
Thallus areolate, whitish gray, becoming yellowish white in the
herbarium; surface smooth, epruinose. Apothecia prominent,
lirellate; lirellae elongate, bent and usually branched, 1–3 mm
6AMERICAN JOURNAL OF BOTANY [Vol. 100
7
May 2013] LÜCKING ET AL.—EVOLUTION OF GRAPHIDACEAE
Ecogeography — Redonographa and Gymnographopsis have
a unique ecogeography within the family Graphidaceae, being
found exclusively on (often volcanic) rocks in coastal semi-
desert to desert environments characterized by dew or fog as
the primary means of precipitation. Redonographa chilensis ,
R. saxiseda , and Gymnographopsis chilena , are known from
the Pacifi c Desert biogeographical province in central and north-
ern Chile ( Dodge, 1966 ; Redón and Follmann, 1972 ; Egea and
Torrente, 1997 ; Bungartz et al., 2010 ; present study): R. chilensis
is known from the Coquimbo, Antofagasta, and Aconcagua Re-
gions, R. saxiseda from the Coquimbo and Aconcagua Regions,
and G. chilena from the Aconcagua Region. Redonographa
saxiseda has also been reported from the Galapagos Islands
( Bungartz et al., 2010 ), but the material represents a distinct spe-
cies, R. galapagoensis (see above). Redonographa saxorum was
originally described from the Sonoran Desert in California and
Baja California ( Egea and Torrente, 1997 ; Staiger and Kalb, 2004 )
and later also reported from the Galapagos Islands ( Bungartz
et al., 2010 ). These areas correspond to the Sonoran, Pacifi c
Desert, and Galapagos biogeographic provinces ( Udvardy, 1975 ),
whereas Gymnographopsis latispora occurs in the Cape Sclero-
phyll biogeographical province bordering the Karoo Desert
( Fig. 5 ). These regions are also commonly known as the Mediter-
ranean regions, besides the California Floristic Province, Central
Chile, and the Cape Floristic region. They also include the Medi-
terranean Basin and southwestern Australia ( Cowling et al., 1996 )
and are considered biodiversity hotspots ( Mittermeier et al., 2005 ).
Ancestral ecogeographical character state analysis — The
Bayesian approach resulted in signifi cant posterior probabilities
for the crown node (most recent common ancestor) of Graphi-
daceae as a whole, the basal node of Redonographoideae plus
Graphidoideae, and the basal node of Graphidoideae, as being
wet tropical (PP = 0.9962 for all nodes). In contrast, the crown
node of Redonographoideae was reconstructed as “mediterra-
nean” with high posterior probability (PP = 1.0).
Dating analysis — The relaxed molecular clock analysis ( Fig. 2 )
allows us to infer a revised crown node age of (171–)148(–119)
Myr for the Graphidaceae and an age for the split between Re-
donographoideae and Graphidoideae of (155–)132(–104) Myr,
as well as a crown node age of (136–)95(–90) Myr for Graphi-
doideae and (32–)25(–9) Myr for Redonographa . These esti-
mates correspond to the (Middle Jurassic: Bajocian to) Early
Cretaceous: Berrisian (to Early Cretaceous: Aptian) for the
Graphidaceae crown node, the (Late Jurassic: Kimmeridgian
to) Early Cretaceous: Hauterivian (to Early Cretaceous: Albian)
for the Redonographoideae-Graphidoideae split, the (Early
Cretaceous: Hauterivian to) Late Cretaceous: Cenomanian (to
Late Cretaceous: Turonian) for the Graphidoideae crown
node, and the (Oligocene: Rupelian to) Oligocene: Chattian
(to Miocene: Tortonian). Thus, the main lineages with Graphi-
daceae appear to have evolved around the Early Cretaceous,
whereas Redonographa diversifi ed comparatively late in the
Oligocene-Miocene.
5a Excipulum basally uncarbonized, lirellae irregularly branched; as-
cospores more or less citriform, with irregular cell lumina (astrothe-
lioid) Redonographa saxiseda
5b Excipulum basally carbonized, lirellae stellately branched to pseu-
dostromatic; ascospores ellipsoid to oval, with regular cell lumina
(graphidoid) Redonographa chilensis
Taxonomy — Based on differences in the arrangement of the
lirellae and ascospore size and shape, accompanied by differ-
ences in distribution and, as far as known, molecular data, we
currently recognize four species of Redonographa , with the cen-
ter of diversity in central and northern Chile. Although no se-
quences are available for Gymnographopsis , the genus agrees
with Redonographa in its ecology and distribution, the ecorticate
thallus, the comparatively stout excipular periphysoids, and the
I-negative, small, mostly (sub)muriform ascospores with thick-
ened septa and lens-shaped to rounded lumina. The overall as-
coma morphology of G. chilena ( Fig. 4G–I ) is indeed very similar
to that of R. chilensis ( Fig. 3B–F ). Both genera differ in excipular
carbonization and secondary chemistry; an unknown compound
has been reported from G. chilena ( Staiger, 2002 ), but based on
spot characteristics, this compound appears to also belong in the
stictic-norstictic acid group. Staiger (2002) considered Gym-
nographopsis to be monospecifi c and apparently overlooked that
a second species had been described by Egea and Torrente (1996)
from South Africa. In fact, there are fi ve names in this genus,
besides the two species accepted here also G. follmannii C. W.
Dodge, G. chilensis (C. W. Dodge) Follm., and G. cerei Follm.
( Follmann, 1967 ). The fi rst is a lapsus generated by the Index
Fungorum (http://www.indexfungorum.org), referring to the spe-
cies Graphis follmannii C. W. Dodge, which was never described
or combined in Gymnographopsis ; it is not related to that genus
but represents a species of Opegrapha (holotype Follmann 14485
in FH checked). The second is a superfl uous replacement name
for Gymnographopsis chilena , erroneously assuming that chilen-
sis must be the correct spelling. The third is a species growing on
cacti, and revision of the type material revealed that it does not
belong in Gymnographopsis ; it resembles the genus Hemithe-
cium , but the I-negative ascospores indicate possible placement
in Fissurina , which contains several species with well-developed
labia ( Staiger, 2002 ).
Three further small genera to be considered here are
Anomalographis , Gymnographa , and Sarcographina ( Kalb
and Hafellner, 1992 ; Staiger, 2002 ; Archer, 2009 ). Anoma-
lographis is based on Graphis madeirensis Tav. ( Tavares,
1952 ); it agrees with Gymnographopsis and Redonographa
in the saxicolous growth habit in Mediterranean ecosystems
and, in part, the norstictic acid chemistry, but its ascus and
ascospore types are different: the ascospores are 1-septate
and have thin walls and septa. In addition, periphysoids are
absent ( Staiger, 2002 ). Both Gymnographa and Sarcograph-
ina have dark brown ascospores with thin septa and walls
and are wet-tropical in their ecology ( Archer, 2009 ). There-
fore, we do not consider these taxa forming part of subfam-
ily Redonographoideae.
Fig. 3. Morphological and anatomical details of species of Redonographa . (A) Habitat of R. chilensis and R. saxiseda along the Pacifi c coast of
Coquimbo province, Chile. (B–G) Redonographa chilensis ; (B, C) general habit of thallus with ascomata (B, Tehler 8407 ; C, Tehler 9887 ); (D–F) details
of thallus and ascomata; (D, E) holotype of Opegrapha petraea ; (F) holotype of Medusulina chilena ); (G) ascospore ( Tehler 9927 ). (H) Habitat of R. galapa-
goensis and R. saxorum on Santiago Island (Galapagos Islands). (I–L) R. galapagoensis (all holotype); (I–J) details of thallus with ascomata; (K) section
through lateral excipulum showing upper layer of verrucose (arrow) periphysoids causing the pruina; (L) detail of verrucose periphysoids. Scale: B–F and
I–J = 1 mm, G = 10 µm, K–L = 5 µm.
←
8AMERICAN JOURNAL OF BOTANY [Vol. 100
family are other examples ( Martín et al., 2003 ; Nelsen et al.,
2010 ; Rivas Plata et al., 2012 , 2013 ). However, many Graphi-
daceae behave differently, in that morphologically or ecologi-
cally unique lineages are phylogenetically close to other lineages,
such as Cruentotrema , the Topeliopsis -like Chapsa meridensis ,
and the mazaediate Nadvornikia hawaiiensis ( Mangold et al.,
2008 ; Rivas Plata and Lumbsch, 2011 ; Rivas Plata et al., 2012 ,
2013 ). Even Diploschistes is nested within Graphidoideae,
DISCUSSION
The new genus Redonographa and the new subfamily Redono-
graphoideae, which also includes the genus Gymnographopsis ,
provide a remarkable example how unique ecogeographical or
morphological features correlate with a peculiar phylogeny in
lichenized fungi. Such a fi nding is not new and the genera
Diploschistes , Heiomasia , and Phaeographopsis in the same
Fig. 4. Morphological and anatomical details of species of Redonographa and Gymnographopsis . (A–E) R. saxiseda ; (A) general habit of thallus with
ascomata ( Tehler 8370 ); (B, C) details of thallus and ascomata (holotype; photographs by Othmar Breuss); (D, E) ascospores inside and outside ascus
( Tehler 8370 ). (F) R. saxorum ( Bungartz 5208 ), details of thallus and ascomata. (J–L) Gymnographopsis chilena (holotype), details of thallus with asco-
mata. Scale: A–C and F–I = 1 mm, D–E = 10 µm.
9
May 2013] LÜCKING ET AL.—EVOLUTION OF GRAPHIDACEAE
and the Mediterranean Basin are unrelated ( Sérusiaux et al.,
2010 ). Tehler et al. (2009a) demonstrated that saxicolous
Roccella in Galapagos consists entirely of endemic species,
probably related to a South American ancestor, whereas the
single epiphytic species reported from Galapagos, Roccella
gracilis , is widespread. In general, saxicolous species found
in the Galapagos Islands appear to be mostly identical or re-
lated to taxa from the Pacifi c desert region in South America,
a phenomenon also found in bryophytes ( Gradstein and Weber,
1982 ).
It thus appears that most saxicolous species and genera
present in the Mediterranean Regions, such as the Atacama
Desert, the Sonoran Desert, and the Galapagos Islands, have a
rather restricted distribution ( Rundel, 1978 ), similar to those
of vascular plants, such as the genus Nolana in the Solanaceae
( Dillon, 2005 ), indicating that these species were unable to
disperse widely across disparate ecosystems such as the An-
des and the Chocoan and Amazon rain forest but instead are
relicts of lineages going back to a Gondwana origin. This is
supported by plant-biogeographic relationships between the
Mediterranean regions, although these are mostly evident be-
tween the Cape Floristic Region and southwestern Australia
( Galley and Linder, 2006 ), between the Mediterranean Basin
and the Cape Floristic Region ( Buerki et al., 2012 ), and be-
tween the California Floristic Province and the Mediterranean
Basin. Only a few vascular plant clades in the Cape Floristic
Province appear to have affi nities to South America ( Galley
and Linder, 2006 ). On the other hand, lichenized fungal lin-
eages such as Diploschistes or representatives of Arthoniales
and Teloschistales are known to be widespread across the Medi-
terranean regions ( Kärnefelt, 1990 ; Guderley and Lumbsch,
1996 ; Egea and Torrente, 1996 ; Lumbsch, 2002 ; Lumbsch and
Elix, 2003 ).
Redonographa also provides yet another example of remark-
able parallel evolution in Graphidaceae, adding to those high-
lighted by Rivas Plata and Lumbsch (2011) , since there are no
straightforward phenotype characters that would distinguish
this taxon from the unrelated Carbacanthographis in subfamily
Graphidoideae ( Staiger, 2002 ; Bungartz et al., 2010 ; Lücking,
2013 ), even if the molecular data put them far apart from each
other. Staiger and Kalb (2004) were the fi rst to recognize the
thicker, mostly smooth periphysoids in “ Graphis ” saxorum vs.
those in Carbacanthographis s.s. This difference is confi rmed
here, but experience is needed to differentiate the thicker, ver-
rucose periphysoids of Redonographa galapagoensis from the
thinner, spinulose periphysoids in Carbacanthographis . Rather
than morphological characters, it seems that substrate and ecol-
ogy, as well as chemistry, are also good indicators to distin-
guish these lineages, a fi nding that also becomes apparent in
other groups of Graphidaceae with molecular data available
( Rivas Plata et al., 2013 ). Most well-defi ned genus-level clades
in this family now have a very well-circumscribed morphology,
chemistry, and ecology. Accordingly, fi eld observations to cor-
rectly delimit these taxa are important.
Several large lichenized lineages are known to have basal or
sister clades with predominantly saxicolous growth in exposed,
warm climates. For example, the largest lichenized clade, Leca-
noromycetes, has subclasses Acarosporomycetidae and Can-
delariomycetidae in a basal position, and these are commonly
found in subtropical deserts on rock ( Hofstetter et al., 2007 ).
Such evolutionary patterns are consistent with estimates that
date Lecanoromycetes back to the warm Triassic ( Amo de Paz
et al., 2011 ; E. Rivas Plata et al., unpublished manuscript ). Also
although its correct position within the subfamily is unresolved
( Martín et al., 2003 ; Fernández-Brime et al., 2011 ; Rivas Plata
et al., 2013 ). The situation in Redonographoideae is different,
since this lineage is the fi rst known supported sister group to
subfamily Graphidoideae.
The distinctive distribution of Redonographoideae in the
Sonoran, Pacifi c Desert, Galapagos, and Cape Sclerophyll
biogeographical provinces is rare for a fungal or lichenized
lineage. On the basis of plant biogeography, the Californian
and Sonoran provinces are part of the Nearctic Realm, whereas
Galapagos and the Pacifi c Desert are part of the Neotropical
Realm, and Cape Sclerophyll belongs to the Afrotropical Realm
( Udvardy, 1975 ). Among Graphidaceae, another rock- and
soil-dwelling genus is Diploschistes , which, however, is sub-
cosmopolitan in distribution and found in temperate, subtrop-
ical, and tropical montane settings ( Lumbsch, 1989 ; Guderley
and Lumbsch, 1996 ; Lumbsch, 2002 ; Lumbsch and Elix,
2003 ). Lichenized fungi with a similar ecology and distribu-
tion as Redonographa and Gymnographopsis include genera
within Arthoniales, such as Dirina , Lecanographa , Roccella ,
and Roccellina ( Tehler, 1983 ; Egea and Torrente, 1996 ; Tehler
and Irestedt, 2007 ; Tehler et al., 2009a , b ), although biogeo-
graphic connections between the Sonoran and Atacama des-
ert seem to be rare. For example, while Roccella and Dirina
occur from California south to Galapagos and northern Peru,
they are replaced further south by Roccellina , which is also
known from South Africa ( Tehler, 1993 , 1996 ; Egea and Torrente,
1996 ; Lohtander et al., 1998 ; Tehler and Irestedt, 2007 ). One
species of Lecanographa , L. subdryophila (Follmann &
Vězda) Egea & Torrente, is known from California and Chile,
but is epiphytic rather than saxicolous, whereas the saxicolous
L. subcaesioides Egea & Torrente has a South American-South
African distribution ( Egea and Torrente, 1994 ) and also occurs
in Galapagos. The mostly epiphytic genus Fulvophyton , a re-
cent segregate of Sclerophyton ( Ertz and Tehler, 2011 ), has two
species present in Baja California and two further species in
Chile. The saxicolous Arthothelium spilomatoides is known
from Peru and Chile, whereas the related Arthothelium galapa-
goense is endemic to the Galapagos Islands. A Sonoran-Pacifi c
Desert distribution is also found in other groups, such as Calo-
placa ( Kärnefelt, 1990 ) and Ramalinaceae, with Niebla ceruchis
known from Baja California and Chile ( Bowler and Marsh, 2004 ).
However, in the latter it was shown that species in Macaronesia
Fig. 5. World distribution of species of Redonographa and Gymnogra-
phopsis . All species occur on coastal (volcanic) rocks in desert fog oases or
otherwise comparatively dry, subtropical coastal areas.
10 AMERICAN JOURNAL OF BOTANY [Vol. 100
LITERATURE CITED
A HMADJIAN , V. 1993 . The lichen symbiosis. John Wiley and Sons, New
York, New York, USA.
A MO DE PAZ , G . , P . CUBAS , P. K. DIVAKAR , H. T. LUMBSCH , AND A . C RESPO .
2011 . Origin and diversifi cation of major clades in parmelioid li-
chens (Parmeliaceae, Ascomycota) during the Paleogene inferred by
Bayesian analysis. PLoS ONE 6 : e28161 .
A PTROOT , A. , AND H. J. M. SIPMAN . 1997 . Diversity of lichenized fungi in
the tropics. In Hyde, K. D. [ed.], Biodiversity of tropical microfungi,
93–106. University Press, Hong Kong.
A RCHER , A. W. 2009 . Graphidaceae. In P. M. McCarthy [ed.], Flora of
Australia, vol. 57 (Lichens 5), 84–194. Australian Biological Resource
Study, Canberra, Australia and Commonwealth Scientifi c Investigation
and Research Organisation Publishing, Melbourne, Australia.
B ALOCH , E . , R . L ÜCKING , H. T. LUMBSCH , AND M . WEDIN . 2010 . Major
clades and phylogenetic relationships between lichenized and non-
lichenized lineages in Ostropales (Ascomycota: Lecanoromycetes).
Taxon 59 : 1483 – 1494 .
B ERBEE , M. L. , AND J. W. TAYLOR . 2010 . Dating the molecular clock in
fungi—How close are we? Fungal Biology Reviews 24 : 1 – 16 .
B LACKBURN , T. M. , AND K. J. GASTON . 1997 . The relationship between
geographic area and the latitudinal gradient in species richness in New
World birds. Evolutionary Ecology 11 : 195 – 204 .
B OKMA , F. J. , AND M . M ONKKONEN . 2001 . Random processes and geo-
graphic species richness patterns: Why so few species in the north?
Ecography 24 : 43 – 49 .
B OLLBACK , J. P. 2006 . SIMMAP: Stochastic character mapping of dis-
crete traits on phylogenies. BMC Bioinformatics 7 : 88 .
B OWLER , P. A. , AND J . E . M ARSH . 2004 . Niebla . In T. H. Nash III, B. D.
Ryan, P. Diederich, C. Gries, and F. Bungartz [eds.], Lichen fl ora of the
Greater Sonoran Desert Region, vol. 2, 368–380. Lichens Unlimited,
Arizona State University, Tempe, Arizona.
B RODO , I. M. , S. D. SHARNOFF , AND S. SHARNOFF . 2001 . Lichens of North
America. Yale University Press, New Haven, Connecticut, USA.
B ROWN , J. H. , AND M . V . LOMOLINO . 1998 . Biogeography. Sinauer, Sunderland,
Massachusetts, USA.
B UERKI , S . , S . J OSE , S. R. YADAV , P . G OLDBLATT , J. C. MANNING , AND F .
F OREST . 2012 . Contrasting biogeographic and diversifi cation patterns
in two Mediterranean-type ecosystems. PLoS ONE 7 : e39377 .
B UNGARTZ , F . , R . L ÜCKING , AND A . APTROOT . 2010 . The lichen fam-
ily Graphidaceae (Ostropales, Lecanoromycetes) in the Galapagos
Islands. Nova Hedwigia 90 : 1 – 44 .
C OWLING , R. M. , P. W. RUNDEL , B. B. LAMONT , M . K . A RROYO , AND M.
A RIANOUTSOU . 1996 . Plant diversity in mediterranean-climate regions.
Trends in Ecology & Evolution 11 : 362 – 366 .
C URRIE , D. J. , G. G. MITTELBACH , H. V. CORNELL , D. M. KAUFMAN , J. T.
K ERR , T . O BERDORFF , AND J.-F. GUGAN . 2004 . Predictions and tests of
climate-based hypotheses of broad-scale variation in taxonomic rich-
ness. Ecology Letters 7 : 1121 – 1134 .
D ILLON , M. O. 2005 . Solanaceae of the Lomas formations of Coastal
Peru and Chile. Annals of the Missouri Botanical Garden 104 :
131 – 155 .
D ODGE , C. W. 1966 . New lichens from Chile. Nova Hedwigia 1 2 :
307 – 352 .
D RUMMOND , A. J. , AND A . RAMBAUT . 2007 . BEAST: Bayesian evolution-
ary analysis by sampling trees. BMC Evolutionary Biology 7 : 214 .
E GEA , J. M. , AND P . T ORRENTE . 1994 . El género de hongos liquenizados
Lecanactis (Ascomycotina). Bibliotheca Lichenologica 54 : 1 – 205 .
E GEA , J. M. , AND P . T ORRENTE . 1996 . Tres nuevas especies de hongos
liquenizados de la Provincia del Cabo (Sudáfrica). Cryptogamie.
Bryologie, Lichenologie 17 : 295 – 312 .
E GEA , J. M. , AND P . TORRENTE . 1997 . Graphis saxorum (lichenized
Ascomycotina, Graphidaceae) a new species from California and Baja
California. The Bryologist 100 : 207 – 209 .
E LDRIDGE , D. 1997 . Caretakers of the desert. Nature Australia 1997 :
48 – 55 .
E RIKSSON , O. E. 2005 . Origin and evolution of Ascomycota—The protoli-
chenes hypothesis. Svensk Mykologisk Tidskrift 26 : 30 – 33 .
the predominantly tropical Arthoniomycetes have a rock-inhab-
iting fungal sister group ( Gueidan et al., 2008 ). With the fi nding
that subfamily Graphidoideae has a rock-inhabiting sister group,
Redonographoideae, it could be hypothesized that this subfam-
ily, or even the entire family, evolved from a saxicolous an-
cestor characteristic of subtropical climates. However, since
the tropical-epiphytic subfamily Fissurinoideae is sister to Re-
donographoideae plus Graphidoideae, the ancestral ecogeogra-
phy state analysis employed here rejects this hypothesis and
instead indicates that the subtropical-saxicolous ecogeography
evolved secondarily within the subfamily. This is supported by
the fact that Graphidaceae, and hence Redonographoideae, are
nested deep within the Ostropales, which are predominantly
wet-tropical ( Kauff and Lutzoni, 2002 ; Lumbsch et al., 2007 ;
Baloch et al., 2010 ). Also, the early divergence dates of Graphi-
daceae as a whole agree with the early evolution of extensive
tropical rain forests in the Early to Middle Jurassic (E. Rivas
Plata et al., unpublished manuscript ), and three of the four sub-
families (Fissurinoideae, Gomphilloideae, Graphidoideae) have
largely or entirely retained this ecology. On the other hand, the
reconstruction of the ecogeography of the common ancestor
of subfamilies Redonographoideae and Graphidoideae is de-
pendent on the internal topology of the latter subfamily. This
topology is presently unresolved, but phylogenetic binning
analysis indicates that the genus Diploschistes , another genus
with predominantly “mediterranean” ecogeography, might oc-
cupy a basal position within Graphidoideae (R. Lücking et al.,
unpublished data). If this is confi rmed, it will change the pic-
ture, since then two subsequent clades, Redonographoideae and
Diploschistes , would share a largely subtropical-saxicolous-
terricolous, “mediterranean” ecogeography, which would then
reconstruct the Redonographoideae-Graphidoideae crown node
as subtropical-saxicolous.
The relatively young crown node age estimate for subfam-
ily Redonographoideae would seem to support the hypothesis
that its saxicolous growth in subtropical coastal dew or fog
deserts could have evolved recently. However, the crown is
only represented by two morphologically closely related spe-
cies. Therefore, the true crown node age of the subfamily, in-
cluding the genus Gymnographa , may go farther back in time,
supporting a more ancient origin of this ecotype. Hartley and
Chong (2002) , Hartley (2003) , and Hartley et al. (2005) pos-
tulate that a desert-like climate has been persistent in the Ata-
cama region since 150 Ma in the Late Jurassic (Tithonian),
making it the oldest desert on earth ( Hartley et al., 2005 ), with
a somewhat wetter climate during the Miocene and a transi-
tion to hyperarid conditions due to the Andean uplift about 19
to 13 Ma ( Rech et al., 2006 ). The extraordinarly dry climate of
the Atacama Desert could cause extremely slow growth and
metabolic rates in lichen associations, particularly crustose
lichens on exposed rock surfaces, which would result in much
lower evolutionary rates due to longer generation times ( Kärnefelt,
1990 ). Even if these lichens are mostly found in dew or fog-
exposed habitats and not in permanently dry areas, their de-
pendence on dew or fog in the early morning hours greatly
reduces net photosynthesis ( Rundel, 1978 ; Lange et al., 1991 ,
2006 , 2008 ). Therefore, it is possible that these lichens indeed
have low substitution rates, with only few species evolving in
this clade over the past 150 Myr. Such slow rates of evolution
would support the hypothesis that the peculiar ecogeography
and morphology of Redonographoideae have evolved as far
back as the split with its sister group Graphidoideae in the
Late Jurassic to Early Cretaceous.
11
May 2013] LÜCKING ET AL.—EVOLUTION OF GRAPHIDACEAE
K ALB , K . , AND J . H AFELLNER . 1992 . Bemerkenswerte Flechten und licheni-
cole Pilze von der Insel Madeira. Herzogia 9 : 45 – 102 .
K APPEN , L. 1982 . Lichen oases in hot and cold deserts. Journal of the
Hattori Botanical Laboratory 53 : 325 – 330 .
K APPEN , L. 1988 . Ecophysiological relationships in different climatic
regions. In M. Galun [ed.], CRC handbook of lichenology, vol. II,
37–100. CRC Press, Boca Raton, Florida, USA.
K ÄRNEFELT , I. 1990 . Evidence of a slow evolutionary change in the spe-
ciation of lichens. Bibliotheca Lichenologica 38 : 291 – 306 .
K ATOH , K . , AND M . T OH . 2005 . MAFFT version 5: Improvement in ac-
curacy of multiple sequence alignment. Nucleic Acids Research 33 :
511 – 518 .
K AUFF , F . , AND F . L UTZONI . 2002 . Phylogeny of Gyalectales and Ostropales
(Ascomycota, Fungi): among and within order relationships based on
nuclear ribosomal RNA small and large subunits. Molecular Phylo-
genetics and Evolution 25 : 138 – 156 .
K ERSHAW , K. A. 1985 . Physiological ecology of lichens. Cambridge
University Press, Cambridge, UK.
K IRK , P. M. , P. F. CANNON , D. W. MINTER , AND J . A . S TALPERS . 2008 .
Dictionary of the Fungi, 10th ed. CABI, Wallingford, UK.
K OLEFF , P. , AND K. J. GASTON . 2001 . Latitudinal gradients in diversity:
Real patterns and random models. Ecography 24 : 341 – 351 .
L ANGE , O. L. , T. G. A. GREEN , B . M ELZER , A . M EYER , AND H . Z ELLNER .
2006 . Water relations and CO 2 exchange of the terrestrial lichen
Teloschistes capensis in the Namib fog desert: Measurements during
two seasons in the fi eld and under controlled conditions. Flora 201 :
268 – 280 .
L ANGE , O. L. , T. G. A. GREEN , A . M EYER , AND H . Z ELLNER . 2008 . Epilithic
lichens in the Namib fog desert: Field measurements of water rela-
tions and carbon dioxide exchange. Sauteria 15 : 283 – 302 .
L ANGE , O . L . , A . M EYER , I . U LLMANN , AND H . Z ELLNER . 1991 . Mikroklima,
Wassergehalt und Photosynthesis von Flechten in der küstennahen
Nebelzone der Namib-Wüste: Messungen während der herbstlichen
Witterungsperiode. Flora 185 : 233 – 266 .
L AWREY , J. D. , R. LÜCKING , H. J. M. SIPMAN , J. L. CHAVES , S. A. REDHEAD ,
F . BUNGARTZ , M . S IKAROODI , AND P. M. GILLEVET . 2009 . High con-
centration of basidiolichens in a single family of agaricoid mush-
rooms (Basidiomycota: Agaricales: Hygrophoraceae). Mycological
Research 113 : 1154 – 1171 .
L IU , Y. J. , S. WHELEN , AND B. D. HALL . 1999 . Phylogenetic relationships
among ascomycetes: Evidence from an RNA polymerase II subunit.
Molecular Biology and Evolution 16 : 1799 – 1808 .
L OHTANDER , K . , M . K ÄLLERSJÖ , AND A . T EHLER . 1998 . Dispersal strategies
in Roccellina capensis (Arthoniales). Lichenologist 30 : 341 – 350 .
L OPEZ-VAAMONDE , C . , N . W IKSTROM , K. M. KJER , G. D. WEIBLEN , J. Y.
R ASPLUS , C. A. MACHADO , AND J. M. COOK . 2009 . Molecular dating
and biogeography of fi g-pollinating wasps. Molecular Phylogenetics
and Evolution 52 : 715 – 726 .
L ÜCKING , R. 2013 . Minksia chilena (C. W. Dodge) Redón & Follmann
belongs in Graphidaceae and its correct name is Carbacanthographis
chilensis (Zahlbr.) Lücking. Lichenologist 45 : 127 – 129 .
L ÜCKING , R . , S . H UHNDORF , D. H. PFISTER , E . R IVAS PLATA , AND H . T .
L UMBSCH . 2009a . Fungi evolved right on track. Mycologia 101 :
810 – 822 .
L ÜCKING , R . , E . R IVAS PLATA , J. L. CHAVES , L . U MAÑA , AND H. J. M. SIPMAN .
2009b . How many tropical lichens are there... really? Bibliotheca
Lichenologica 100 : 399 – 418 .
L UMBSCH , H. T. 1989 . Die holarktischen Vertreter der Flechtengattung
Diploschistes (Thelotremataceae). Journal of the Hattori Botanical
Laboratory 66 : 133 – 196 .
L UMBSCH , H. T. 2002 . Diploschistes . In T. H. Nash III, B. D. Ryan, C.
Gries, and F. Bungartz [ed.], Lichen fl ora of the Greater Sonoran Desert
Region, vol. I, 173–178. Lichens Unlimited, Arizona State University,
Tempe, Arizona, USA.
L UMBSCH , H. T. , AND J . A . E LIX . 2003 . The lichen genus Diploschistes
(Thelotremataceae) in Australia. Bibliotheca Lichenologica 86 :
119 – 128 .
L UMBSCH , H . T . , I . S CHMITT , R . L ÜCKING , E . W IKLUND , AND M . W EDIN . 2007 .
The phylogenetic placement of Ostropales within Lecanoromycetes
(Ascomycota) revisited. Mycological Research 111 : 257 – 267 .
E RTZ , D . , AND A . T EHLER . 2011 . The phylogeny of Arthoniales
(Pezizomycotina) inferred from nucLSU and RPB2 sequences. Fungal
Diversity 49 : 47 – 71 .
F ARRIS , J. S. , V. A. ALBERT , M . K ÄLLERSJÖ , D. L. LIPSCOMB , AND A. G.
K LUGE . 1996 . Parsimony jackknifi ng outperforms neighbor-joining.
Cladistics 12 : 99 – 124 .
F ERNÁNDEZ-BRIME , S. , X. LLIMONA , K. MOLNAR , S . STENROOS , F . HÖGNABBA ,
C . B JÖRK , F . L UTZONI , AND E . G AYA . 2011 . Expansion of the
Stictidaceae by the addition of the saxicolous lichen-forming genus
Ingvariella. Mycologia 103 : 755 – 763 .
F OLLMANN , G. 1967 . Die Flechtenfl ora der nordchilenischen Nebeloase
Cerro Moreno. Nova Hedwigia 14 : 215 – 281 .
F RIEDMANN , E. I. , AND M . G ALUN . 1974 . Desert algae, lichens, and fungi.
In G. W. Brown [ed.], Desert biology, vol. II, 165–212. Academic
Press, New York, New York, USA.
F RISCH , A . , K . K ALB , AND M . G RUBE . 2006 . Contributions towards a
new systematics of the lichen family Thelotremataceae. Bibliotheca
Lichenologica 92 : 1 – 539 .
G ALLEY , C . , AND H. P. LINDER . 2006 . Geographical affi nities of the Cape
fl ora, South Africa. Journal of Biogeography 33 : 236 – 250 .
G ARGAS , A. , P. T. DEPRIEST , M . G RUBE , AND A . T EHLER . 1995 . Multiple
origins of lichen symbioses in fungi suggested by SSU rDNA phylog-
eny. Science 268 : 1492 – 1495 .
G ASTON , K. J. 2000 . Global patterns in biodiversity. Nature 405 : 220 – 227 .
G OLOBOFF , P. A. , J. S. FARRIS , AND K . C . N IXON . 2008 . TNT, a free pro-
gram for phylogenetic analysis. Cladistics 24 : 774 – 786 .
G RADSTEIN , S. R. , AND W. A. WEBER . 1982 . The bryogeography of the
Galapagos Islands. Journal of the Hattori Botanical Laboratory 52 :
127 – 152 .
G UDERLEY , R . , AND H . T . L UMBSCH . 1996 . The lichen genus Diploschistes
in South Africa (Thelotremataceae). Mycotaxon 58 : 269 – 292 .
G UEIDAN , C . , C . R UIBAL VILLASEÑOR , G. S. DE HOOG , A. A. GORBUSHINA , W .
A. UNTEREINER , AND F . L UTZONI . 2008 . A rock-inhabiting ancestor for
mutualistic and pathogen-rich fungal lineages. Studies in Mycology
61 : 111 – 119 .
H ALE , M. E. JR . 1974 . Morden-Smithsonian expedition to Dominica: The
lichens (Thelotremataceae). Smithsonian Contributions to Botany 16 :
1 – 46 .
H ALE , M. E. JR . 1978 . A revision of the lichen family Thelotremataceae in
Panama. Smithsonian Contributions to Botany 38 : 1 – 60 .
H ALE , M. E. JR . 1981 . A revision of the lichen family Thelotremataceae in
Sri Lanka. Bulletin of the British Museum of Natural History (Botany)
8 : 227 – 332 .
H ALL , T. A. 1999 . BioEdit: A user-friendly biological sequence align-
ment editor and analysis program for Windows 95/98/NT. Nucleic
Acids Symposium Series 41 : 95 – 98 .
H ARTLEY , A. J. 2003 . Andean uplift and climate change. Geological
Society of London Journal 160 : 7 – 10 .
H ARTLEY , A. J. , AND G . C HONG . 2002 . Late Pliocene age for the Atacama:
Implications for desertifi cation of western South America. Geology
30 : 43 – 46 .
H ARTLEY , A. J. , G. CHONG , J . H OUSTON , AND A. E. MATHER . 2005 . 150
Million years of climate stability: Evidence from the Atacama Desert,
northern Chile. Geological Society of London Journal 162 : 421 – 444 .
H AWKSWORTH , D. L. 2005 . Life-style choices in lichen-forming and li-
chen-dwelling fungi. Mycological Research 109 : 135 – 136 .
H ILLEBRAND , H. 2004 . On the generality of the latitudinal diversity gradi-
ent. American Naturalist 163 : 192 – 211 .
H OFSTETTER , V . , J . M IADLIKOWSKA , F. K AUFF , AND F . L UTZONI . 2007 . Phylo-
genetic comparison of protein-coding versus ribosomal RNA-coding
sequence data: A case study of the Lecanoromycetes (Ascomycota).
Molecular Phylogenetics and Evolution 44 : 412 – 426 .
H UELSENBECK , J. P. , R . NIELSEN , AND J . P . B OLLBACK . 2003 . Stochastic
mapping of morphological characters. Systematic Biology 5 2 :
131 – 158 .
H UNECK , S . , AND G . FOLLMANN . 1967 . Zur Chemie chilenischer
Flechten XV. Über die Inhaltsstoffe von Ramalina cactacearum
Follm., R. ecklonii (Spreng.) Mey. et Flot. var. ambigua Mont. und
Medusulina chilena Dodge. Zeitschrift für Naturforschung 22B :
110 – 111 .
12 AMERICAN JOURNAL OF BOTANY [Vol. 100
P EREIRA , A. B. , A. A. SPIELMANN , M. F. N. MARTINS , AND M . R . F RANCELINO .
2007 . Plant communities form ice-free areas of Keller Peninsula,
King George Island, Antarctica. Oecologia Brasiliensis 11 : 14 – 22 .
R ECH , J. A. , B. S. CURRIE , G. MICHALSKI , AND A. M. COWAN . 2006 .
Neogene cli mate change and uplift in the Atacama Desert, Chile.
Geology 34 : 761 – 764 .
R EDÓN , J. 1973 . Beobachtungen zur Geographie und Okologie der
Chilenischen Flechtenfl ora. Journal of the Hattori Botanical Laboratory
37 : 153 – 167 .
R EDÓN , J. 1974 . Observaciones sistematicas y ecologicas en liquenes
del parque nacional “Vicente Perez Rosales”. Anales del Museo de
Historia Natural de Valparaiso 1974 : 169 – 225 .
R EDÓN , J. 1982 . Lichens of arid South America. Journal of the Hattori
Botanical Laboratory 53 : 337 – 339 .
R EDÓN , J . , AND G . F OLLMANN . 1972 . Beobachtungen zur Verbreightung
chilenischer Flechten. V. Minksia chilensis (Dodge) Redon & Follm.
Philippia 1 : 132 – 136 .
R EDÓN , J . , AND O . L . L ANGE . 1983 . Epiphytische Flechten im Bereich
einer Chilenischen “Nebeloase” (Fray Jorge). I. Vegetationskundliche
Gliederung und Standortsbedingungen. Flora 174 : 213 – 243 .
R ETALLACK , G. J. 1994 . Were the Ediacaran fossils lichens? Paleobiology
20 : 523 – 544 .
R ETALLACK , G. J. 1995 . Ediacaran lichens—A reply to Waggoner.
Paleobiology 21 : 398 – 399 .
R ETALLACK , G. J. 2007 . Growth, decay and burial composition of
Dickinsonia , an iconic Ediacaran fossil. Alcheringa 31 : 215 – 240 .
R IVAS PLATA , E . , AND R . L ÜCKING . 2013 . High diversity of Graphidaceae (Asco-
mycota: Ostropales) in Amazonian Peru. Fungal Diversity 58 : 13 – 32 .
R IVAS PLATA , E . , R . L ÜCKING , AND H. T. LUMBSCH . 2008 . When family
matters: An analysis of Thelotremataceae (Lichenized Ascomycota:
Ostropales) as bioindicators of ecological continuity in tropical for-
ests. Biodiversity and Conservation 17 : 1319 – 1351 .
R IVAS PLATA , E . , AND H. T. LUMBSCH . 2011 . Parallel evolution and phe-
notypic disparity in lichenized fungi: A case study in the lichen-form-
ing fungal family Graphidaceae (Ascomycota: Lecanoromycetes:
Ostropales). Molecular Phylogenetics and Evolution 61 : 45 – 63 .
R IVAS PLATA , E . , H. T. LUMBSCH , AND R . L ÜCKING . 2012 . A new clas-
sifi cation for the lichen family Graphidaceae s.lat. (Ascomycota:
Lecanoromycetes: Ostropales). Fungal Diversity 52 : 107 – 121 .
R IVAS PLATA , E . , S . PARNMEN , B . STAIGER , A. MANGOLD , A . FRISCH , G .
W EERAKOON , J. E. HERNÁNDEZ M. , ET AL . 2013 . A molecular phy-
logeny of Graphidaceae (Ascomycota: Lecanoromycetes: Ostropales)
including 427 species. MycoKeys : in press .
R OHDE , K. 1992 . Latitudinal gradients in species diversity: The search for
the primary cause. Oikos 65 : 514 – 527 .
R UNDEL , P. W. 1978 . Ecological relationships of desert fog zone lichens.
Bryologist 81 : 277 – 293 .
S CHOCH , C. L. , G.-H. SUNG , F . L ÓPEZ-GIRÁLDEZ , J . P . T OWNSEND , J .
M IADLIKOWSKA , V. HOFSTETTER , B . R OBBERTSE , ET AL . 2009 . The
Ascomycota tree of life: A phylum-wide phylogeny clarifi es the ori-
gin and evolution of fundamental reproductive and ecological traits.
Systematic Biology 58 : 224 – 239 .
S ÉRUSIAUX , E . , P . V AN DEN BOOM , AND D . E RTZ . 2010 . A two-gene phy-
logeny shows the lichen genus Niebla (Lecanorales) is endemic
to the New World and does not occur in Macaronesia nor in the
Mediterranean basin. Fungal Biology 114 : 528 – 537 .
S IPMAN , H. J. M. , R . LÜCKING , A. APTROOT , J. L. CHAVES , K . KALB , AND L.
U MAÑA TENORIO . 2012 . A fi rst assessment of the Ticolichen biodi-
versity inventory in Costa Rica and adjacent areas: The thelotremoid
Graphidaceae (Ascomycota: Ostropales). Phytotaxa 55 : 1 – 214 .
S TAIGER , B. 2002 . Die Flechtenfamilie Graphidaceae. Studien in Richtung
einer natürlicheren Gliederung. Bibliotheca Lichenologica 85 : 1 – 526 .
S TAIGER , B. , AND K . K ALB . 2004 . Graphis . In T. H. Nash, III, B. D. Ryan,
P. Diederich, C. Gries, and F. Bungartz [eds.], Lichen fl ora of the
Greater Sonoran Desert Region, vol. 2, 118–122. Lichens Unlimited,
Arizona State University, Tempe, Arizona, USA.
S TAMATAKIS , A. 2006 . RAxML-VI-HPC: Maximum-likelihood-based
phylogenetic analyses with thousands of taxa and mixed models.
Bioinformatics 22 : 2688 – 2690 .
L UTZONI , F . , M . P AGEL , AND V . REEB . 2001 . Major fungal lineages are de-
rived from lichen symbiotic ancestors. Nature 411 : 937 – 940 .
M ANGOLD , A . , M . P . M ARTIN , R . L ÜCKING , AND H . T . L UMBSCH . 2008 .
Molecular phylogeny suggests synonymy of Thelotremataceae within
Graphidaceae (Ascomycota: Ostropales). Taxon 57 : 476 – 486 .
M ARTÍN , M. P. , S. LAGRECA , AND H. T. LUMBSCH . 2003 . Molecular phylog-
eny of Diploschistes inferred from ITS sequence data. Lichenologist
(London, England) 35 : 27 – 32 .
M ASON-GAMER , R. J. , AND E. A. KELLOGG . 1996 . Testing for phylogenetic
confl ict among molecular data sets in the tribe Triticeae (Gramineae).
Systematic Biology 45 : 524 – 545 .
M IADLIKOWSKA , J . , F . KAUFF , V . H OFSTETTER , E . F RAKER , M . G RUBE , J .
H AFELLNER , V . REEB , ET AL . 2006 . New insights into classifi cation
and evolution of the Lecanoromycetes (Pezizomycotina, Ascomycota)
from phylogenetic analyses of three ribosomal RNA- and two protein-
coding genes. Mycologia 98 : 1088 – 1103 .
M IADLIKOWSKA , J . , AND F . L UTZONI . 2000 . Phylogenetic revision of
the genus Peltigera (lichen-forming Ascomycota) based on mor-
phological, chemical and large subunit nuclear ribosomal DNA data.
International Journal of Plant Sciences 161 : 925 – 968 .
M ILLER , M. A. , W. PFEIFFER , AND T . S CHWARTZ . 2010 . Creating the
CIPRES Science Gateway for inference of large phylogenetic trees.
In Proceedings of the Gateway Computing Environments Workshop
(GCE): 1–8. Curran Associates, New Orleans, Louisiana, USA.
M ITTERMEIER , R. A. , P. R. GIL , M . HOVMAN , J . P ILGRIM , T . B ROOKS , ET AL .
2005 . Hotspots revisited: Earth’s biologically richest and most
threatened terrestrial ecoregions. Agrupación Sierra Madre, Mon-
terrey, Mexico.
M ONTAGNE , C. 1852 . Plantas cellulares. Lichenes. Historia Fisica et
Politica de Chile. Museo de Historia Natural de Santiago, Santiago,
Chile.
N ASH , T. H. III [ed.]. 2008 . Lichen biology, 2nd ed. Cambridge University
Press, Cambridge, UK.
N ASH , T. H. III , C. GRIES , AND F . B UNGARTZ . 2007 . Lichen fl ora of the
Greater Sonoran Desert Region, vol. 3. Lichens Unlimited, Arizona
State University, Tempe, Arizona, USA.
N ASH , T. H. III , B. D. RYAN , C . G RIES , AND F. BUNGARTZ [eds.]. 2002 .
Lichen fl ora of the Greater Sonoran Desert Region, vol. 1. Lichens
Unlimited, Arizona State University, Tempe, Arizona, USA.
N ASH , T. H. III , B. D. RYAN , P . D IEDERICH , C . G RIES , AND F. BUNGARTZ
[eds.]. 2004 . Lichen fl ora of the Greater Sonoran Desert Region,
vol. 2. Lichens Unlimited, Arizona State University, Tempe, Arizona,
USA.
N ELSEN , M. P. , R. LÜCKING , M . G RUBE , J. S. MBATCHOU , L . M UGGIA , E .
R IVAS PLATA , AND H. T. LUMBSCH . 2009 . Unravelling the phyloge-
netic relationships of lichenised fungi in Dothideomyceta. Studies in
Mycology 64 : 135 – 144 .
N ELSEN , M. P. , R. LÜCKING , J . S . M BATCHOU , C. J. ANDREW , A. A. SPIELMANN ,
AND H. T. LUMBSCH . 2011 . New insights into relationships of lichen-
forming Dothideomycetes. Fungal Diversity 51 : 155 – 162 .
N ELSEN , M. P. , R. LÜCKING , E . RIVAS PLATA , AND J. S. MBATCHOU . 2010 .
Heiomasia , a new genus in the lichen-forming family Graphidaceae
(Ascomycota: Lecanoromycetes: Ostropales) with disjunct distribu-
tion in southeastern North America and Southeast Asia. Bryologist 113 :
742 – 751 .
N YLANDER , W. 1855 . Additamentum ad fl oram cryptogamicam Chilensem,
quo lichenes praecipue saxicolas exponit. Annales des Sciences
Naturelles 3 : 145 – 187 .
O RANGE , A. , P. W. JAMES , AND F. J. WHITE . 2001 . Microchemical methods
for the identifi cation of lichens. British Lichen Society, London.
Ø VSTEDAL , D. O. , AND R. I. L. SMITH . 2001 . Lichens of Antarctica and
South Georgia. A guide to their identifi cation and ecology. Cambridge
University Press, Cambridge, UK.
P ENN , O . , E . P RIVMAN , H . A SHKENAZY , G . L ANDAN , D . G RAUR , AND T . PUPKO .
2010b . GUIDANCE: A web server for assessing alignment confi -
dence scores. Nucleic Acids Research 38 : W23 – W28 .
P ENN , O . , E . P RIVMAN , G . L ANDAN , D . G RAUR , AND T . P UPKO . 2010a . An
alignment confi dence score capturing robustness to guide-tree uncer-
tainty. Molecular Biology and Evolution 27 : 1759 – 1767 .
13
May 2013] LÜCKING ET AL.—EVOLUTION OF GRAPHIDACEAE
S TAMATAKIS , A . , P . H OOVER , AND J . R OUGEMONT . 2008 . A fast bootstrap-
ping algorithm for the RAxML web-servers. Systematic Biology 57 :
758 – 771 .
S TAMATAKIS , A . , T . L UDWIG , AND H . M EIER . 2005 . RAxML-III: A fast
program for maximum likelihood-based inference of large phyloge-
netic trees. Bioinformatics 21 : 456 – 463 .
T AVARES , C. N. 1952 . Contributions to the lichen fl ora of Macaronesia. I.
Lichens from Madeira. Portugaliae Acta Biologica, B 3 : 308 – 391 .
T AYLOR , T. N. , H. HASS , AND H . K ERP . 1997 . A cyanolichen from the
lower Devonian Rhynie Chert. American Journal of Botany 8 4 :
992 – 1004 .
T EHLER , A. 1983 . The genera Dirina and Roccellina. Opera Botanica 70 :
1 – 86 .
T EHLER , A. 1993 . The genus Sigridea (Roccellaceae, Arthoniales,
Euascomycetidae). Nova Hedwigia 57 : 417 – 435 .
T EHLER , A. 1996 . Syncesia (Arthoniales, Euascomycetidae). Flora
Neotropica 74 : 1 – 48 .
T EHLER , A . , AND M . I RESTEDT . 2007 . Parallel evolution of lichen growth
forms in the family Roccellaceae (Arthoniales, Ascomycota). Cladistics
23 : 432 – 454 .
T EHLER , A . , M . I RESTEDT , F . B UNGARTZ , AND M . W EDIN . 2009a . Evolution
and reproduction modes in the Roccella galapagoensis aggregate
(Roccellaceae, Arthoniales). Taxon 58 : 438 – 456 .
T EHLER , A . , M . I RESTEDT , M . W EDIN , AND D . ERTZ . 2009b . Origin, evolution
and taxonomy of American Roccella (Roccellaceae, Ascomycetes).
Systematics and Biodiversity 7 : 307 – 317 .
T EHLER , A. , D. LITTLE , AND J. S. FARRIS . 2003 . The full-length phylogenetic
tree from 1551 ribosomal sequences of chitinous fungi. Mycological
Research 107 : 901 – 916 .
U DVARDY , M. D. F. 1975 . A classifi cation of the biogeographical prov-
inces of the world. IUCN Occasional Paper no. 18. International
Union for Conservation of Nature, Morges, Switzerland.
V ILGALYS , R . , AND M . H ESTER . 1990 . Rapid genetic identifi cation and
mapping of enzymatically amplifi ed ribosomal DNA from several
Cryptococcus species. Journal of Bacteriology 172 : 4238 – 4246 .
W ILLIG , M. R. , D. M. KAUFMANN , AND R. D. STEVENS . 2003 . Latitudinal
gradients of biodiversity: Pattern, process, scale and synthesis. Annual
Review of Ecology and Systematics 34 : 273 – 309 .
W IRTH , M. , AND M. E. HALE JR . 1963 . The lichen family Graphidaceae in
Mexico . Contributions from the U.S. National Herbarium 36 : 63 – 119 .
W IRTH , M . , AND M . E . H ALE J R . 1978 . Morden-Smithsonian Expedition to
Dominica: The lichens (Graphidaceae). Smithsonian Contributions to
Botany 40 : 1 – 64 .
W IRTH , V. 2010 . Lichens of the Namib Desert: A guide to their identifi ca-
tion. Hess, Göttingen, Germany.
Y UAN , X . , S . X IAO , AND T . N . T AYLOR . 2005 . Lichen-like symbiosis 600
million years ago. Science 308 : 1017 – 1020 .
Z AHLBRUCKNER , A. 1923 . Catalogus lichenum universalis 2. Borntraeger,
Leipzig, Germany.
Z OLLER , S . , C . S CHEIDEGGER , AND C . S PERISEN . 1999 . PCR primers for
the amplifi cation of mitochondrial small subunit ribosomal DNA of
lichen-forming ascomycetes. 31 : 511 – 516 .
