American Journal of Botany 97(9): 1532–1554. 2010.
A PHYLOGENY AND CLASSIFICATION OF THE MUHLENBERGIINAE
(POACEAE: CHLORIDOIDEAE: CYNODONTEAE) BASED ON
PLASTID AND NUCLEAR DNA SEQUENCES1
Paul M. Peterson2,5, Konstantin Romaschenko2,3, and Gabriel Johnson4
2Smithsonian
Institution, Department of Botany MRC-166, National Museum of Natural History, Washington, D.C. 20013-7012
USA; 3Laboratory of Molecular Systematics, Botanic Institute of Barcelona (CSIC−ICUB), Passeig del Migdia, s.n. 08038
Barcelona, Spain; and 4Department of Botany and Laboratories of Analytical Biology, Smithsonian Institution, Suitland,
Maryland 20746 USA
• Premise of the study: To understand the origins of C4 grasslands, we must have a better interpretation of plant traits via phylogenetic reconstruction. Muhlenbergiinae, the largest subtribe of C4 grasses in Mexico and the southwestern United States (with
176 species), is taxonomically poorly understood.
• Methods: We conducted a phylogenetic analysis of 47 genera and 174 species using six plastid regions (ndhA intron, ndhF,
rps16-trnK, rps16 intron, rps3, and rpl32-trnL) and the nuclear ITS 1 and 2 (ribosomal internal transcribed spacer) regions to
infer evolutionary relationships and revise the classification.
• Key results: In our analyses, Muhlenbergia (ca. 153 species) is paraphyletic, with nine genera (Aegopogon, Bealia, Blepharoneuron, Chaboissaea, Lycurus, Muhlenbergia, Pereilema, Redfieldia, Schaffnerella, and Schedonnardus) found nested within.
We recognized the following five well-supported monophyletic lineages within Muhlenbergia: subg. Muhlenbergia, with species that have phosphoenolpyruvate carboxykinase-like leaf anatomy and long, scaly rhizomes; subg. Trichochloa with longlived species that are relatively tall (up to 3 m); subg. Clomena with 3-nerved upper glumes; sect. Pseudosporobolus species
with narrow panicles and plumbeous spikelets; and sect. Bealia species with lemmas with hairy margins and midveins.
• Conclusions: We propose expanding the circumscription of Muhlenbergia to include the other nine genera in this subtribe and
make the following new combinations: Muhlenbergia subg. Bealia, M. diandra, M. geminiflora, M. paniculata, M. phleoides,
M. subg. Pseudosporobolus (also lectotipified), M. solisii, M. tricholepis. We also propose several new names: M. ammophila,
M. columbi, M. plumosa. Our phylograms suggest that Muhlenbergia originated in North America because the sister (Sohnsia
filifolia and Scleropogoninae) is composed of predominantly North American species.
Key words: biogeography; Chloridoideae; classification; ITS; Muhlenbergia; Muhlenbergiinae; phylogeny; plastid DNA
sequences; Poaceae.
Grassland ecosystems are one of the most easily recognized
biomes in the world, covering about 40% of the earth’s surface (World Resources, 2000; Gibson, 2009), and they are also
threatened and highly endangered. Humans evolved with grasslands, and we depend on grasses and grasslands for our sustenance directly as crops (rice, corn, and wheat) and indirectly as
forage for herbivores. However, only a small fraction of grassland ecosystems remains intact today, and we need to study the
biodiversity of this important biome from an evolutionary perspective before it is destroyed.
The Muhlenbergiinae Pilg. is a diverse assemblage of C4
grasses containing 176 species that dominate grasslands in the
western hemisphere. Species such as Muhlenbergia montana
(Nutt.) Hitchc. (mountain muhly) and M. rigida (Kunth) Kunth
1
Manuscript received 19 November 2009: revision accepted 7 July 2010.
The authors thank the National Geographic Society Committee for
Research and Exploration, grant number 8087-06 for field support, the
Smithsonian Institution’s Restricted Endowments Fund, National Museum
of Natural History Small Grants Fund, the Scholarly Studies Program,
Research Opportunities, Atherton Seidell Foundation, and Biodiversity
Surveys and Inventories Program for financial support, J. H. Kirkbride, Jr.
for translating German, A. Touwaide for correcting the Latin, and two
anonymous reviewers for suggesting improvements.
5 Author for correspondence (e-mail: peterson@si.edu)
doi:10.3732/ajb.0900359
(purple muhly) are the most common grass species of highplateau grasslands in north central Mexico, the southwestern
United States, and, to a lesser extent, along the Andean Cordillera of South America. Yet evolutionary relationships and a
modern classification of the Muhlenbergiinae based on the
study of molecular characters have not been completed. To understand the origins and rise of C4 grasslands, a better interpretation of plant traits via phylogenetic reconstruction is essential
(Edwards et al., 2010).
The placement of Muhlenbergia Schreb. within the grasses
has been the subject of many papers since the genus was included in the subfamily Festucoideae, tribe Agrostideae by
Hitchcock (1935) [see Table 1 for a summary of taxonomic
treatments in the Muhlenbergiinae]. The subtribe Muhlenbergiinae was first circumscribed by Pilger (1956) where he recognized a single genus, Muhlenbergia with the following eight
sections: Acroxis (Trin.) Bush, Bealia (Scribn.) Pilg., Cinnastrum
(E. Fourn.) Pilg., Clomena (P. Beauv.) Pilg., Muhlenbergia,
Podosemum (Desv.) Pilg., Pseudosporobolus Parodi, and Stenocladium (Trin.) Bush. In this same treatment, Pilger recognized the genus Epicampes J. Presl (included in subtribe
Sporobolinae Ohwi by Pilger), a name now placed in synonymy
within Muhlenbergia. Subsequent authors have agreed that
Pilger’s infrageneric treatment of Muhlenbergia was not phylogenetically informative (Soderstrom, 1967; Pohl, 1969; Morden,
1985; Peterson and Annable, 1991). With the accumulation of
American Journal of Botany 97(9): 1532–1554, 2010; http://www.amjbot.org/ © 2010 Botanical Society of America
1532
September 2010]
Peterson et al.—Phylogeny of Muhlenberginiinae
Table 1.
Primary taxonomic treatments found in the Muhlenbergiinae
and the number of species in each taxon.
Author
Hitchcock, 1935
Pilger, 1956
Soderstrom, 1967
Pohl, 1969
Türpe 1973
J. Reeder, 1976
C. Reeder, 1985
Peterson, 1989b
Peterson and Annable, 1990
Peterson and Annable, 1991
Peterson and Annable, 1992
Morden and Hatch, 1996
Herrera Arrieta, 1998
Peterson, 2000
Columbus et al., 2002
Taxa treated
Muhlenbergia, USA and Mexico
Muhlenbergiinae with 8 sections
Muhlenbergia subg. Podosemum
(=Trichochloa) sect. Epicampes
Muhlenbergia subg. Muhlenbergia
Aegopogon
Redfieldia
Lycurus
Bealia
Blepharoneuron
“annual” species of Muhlenbergia
Chaboissaea
Muhlenbergia repens complex
Muhlenbergia montana complex
Muhlenbergiinae with 6 genera
Schaffnerella
No. of
species
110
—
26
12
3
1
3
1
2
29
4
6
15
165
1
other types of data, i.e., leaf and embryo anatomy, Muhlenbergia
became firmly placed in the Chloridoideae, although it has been
aligned in a variety of tribes/subtribes, including Eragrostideae
and Sporobolinae (Reeder, 1957; Stebbins and Crampton, 1961;
Clayton and Renvoize, 1986; Peterson et al., 1995, 1997).
Species within the Muhlenbergiinae are morphologically
highly variable and can be characterized as having membranous
ligules (rarely a line of hairs); paniculate inflorescences that are
rebranched or composed only of primary branches; spikelets
that are usually solitary but sometimes in pairs or triads, with
cleistogenes (self-pollinated flowers that do not open at maturity) occasionally present in the leaf sheaths; one floret (rarely
more) per spikelet that is perfect, staminate, or sterile; glumes
that are awned or unawned; lemmas 3-nerved, awned or unawned; and a base chromosome number of x = 8−10 (Peterson
et al., 1995, 1997, 2007a, b; Peterson, 2000). Two subtypes of
C4 photosynthesis based on nicotinamide adenine dinucleotide
cofactor malic enzyme (NAD-ME) and phosphoenolpyruvate
carboxykinase (PCK) have been found in the Muhlenbergiinae
with a few verified by biochemical assay (Gutierrez et al., 1974;
Brown, 1977; Hattersley and Watson, 1992).
On the basis of anatomy, morphology, and cytology, Soderstrom (1967) distinguished two subgenera within Muhlenbergia and divided M. subg. Podosemum (Desv.) Soderstr. (=M.
subg. Trichochloa A. Gray, an older name) into two sections,
sect. Podosemum (Desv.) Pilg. and sect. Epicampes (J. Presl)
Soderstr. Two years later, Pohl (1969) completed a revision of
12 closely related species that he believed represented the entire
M. subg. Muhlenbergia in North America. Based on anatomy,
morphology, cytology, and flavonoid chemistry, 29 annual species of Muhlenbergia have been investigated and placed in tentative natural groups (Peterson and Rieseberg, 1987; Peterson,
1988a, b, 1989a; Peterson et al., 1989; Peterson and Annable,
1991). Morden and Hatch (1987, 1996) investigated the anatomical and morphological variation of six species they referred
to as the M. repens complex. A biosystematics study investigating the M. montana complex (consisting of 15 species) has been
completed (Herrera and Grant, 1993, 1994; Herrera Arrieta,
1998). Molecular genetic data of intersimple sequence repeats
(ISSRs) were investigated for M. capillaris (Lam.) Trin., M.
expansa (Poir.) Trin., and M. sericea (Michx.) P. M. Peterson
(Gustafson and Peterson, 2007).
1533
The Muhlenbergiinae currently consists of 10 genera: Aegopogon (four spp. in North and South America; Türpe, 1973;
Levin and Moran, 1989), Bealia (one sp., B. mexicana Scribn.
in northern Mexico; Peterson, 1989b; Peterson et al., 1993),
Blepharoneuron [two spp. in North America, B. shepherdii
(Vasey) P. M. Peterson & Annable and B. tricholepis (Torr.)
Nash, the latter an important range grass in the southwestern USA
and northern Mexico; Peterson and Annable, 1990, 2003],
Chaboissaea [four spp., three in central Mexico and C. atacamensis
(Parodi) P. M. Peterson & Annable in Argentina and Bolivia;
Peterson and Annable, 1992; Peterson and Herrera Arrieta,
1995; Sykes et al., 1997], Lycurus [three spp., including the
amphitropical disjunct L. setosus (Nutt.) C. Reeder; Peterson
and Morrone, 1998], Muhlenbergia [147 spp. centered in northern Mexico and the southwestern USA, containing the important range grass M. montana and the amphitropical disjuncts M.
arenicola Buckley and M. torreyi (Kunth) Hitchc. ex Bush;
Peterson and Ortíz Diaz, 1998; Peterson, 2003; Herrera Arrieta
and Peterson, 2007; Peterson et al., 2007b; but also with seven
species located in southeast Asia; Wu and Peterson, 2006];
Pereilema (four spp. in North, Central, and South America),
Redfieldia [one sp., R. flexuosa (Thurb. ex A. Gray) Vasey in
the southwestern USA, of probable hybrid origin; Reeder, 1976;
Duvall et al., 1994], Schaffnerella [one sp., S. gracilis (Benth.)
Nash in San Luis Potosí, Mexico; Columbus et al., 2002], and
Schedonnardus [one sp., S. paniculatus (Nutt.) Trel., an amphitropical disjunct with spicate primary inflorescence branches].
Ninety-six percent of the species within the Muhlenbergiinae
are native to the western hemisphere, and more than 80% of
these are native to North America (Peterson et al., 2007a). Amphitropical disjuncts within the Muhlenbergiinae thus far tested
have been shown to have North American origins (Peterson and
Herrera Arrieta, 1995; Sykes et al., 1997; Peterson and Morrone,
1998; Peterson and Ortíz Diaz, 1998; Peterson et al., 2007a).
Within Muhlenbergia, there are 127 species indigenous to
North America (86%); 125 of these occur in Mexico (center of
species diversity) and, of these, 56 are endemic (Peterson
et al., 2007a).
In preliminary molecular analyses, Muhlenbergia has appeared
paraphyletic, with all nine remaining genera of Muhlenbergiinae nested within (Duvall et al., 1994; Hilu and Alice, 2001;
Columbus et al., 2007, 2010; Peterson et al., 2010). Plastid
restriction site markers supported the inclusion of Bealia
Scribn., Blepharoneuron Nash, Chaboissaea E. Fourn., Lycurus,
Pereilema J. Presl, and Redfieldia Vasey in the same subtribe as
Muhlenbergia (Duvall et al., 1994). Columbus et al. (1998) found
that Aegopogon Humb. & Bonpl. ex Willd. and Schaffnerella
Nash, traditionally placed near Bouteloua Lag., actually were
closely aligned with the large genus Muhlenbergia. What is
quite unusual about these two genera is that they do not at first
appear morphologically similar to Muhlenbergia. Aegopogon
has spikelets in triads with the central sessile floret perfect and
the two lateral pedicelled florets staminate or sterile. Muhlenbergia has only solitary spikelets. Hilu and Alice (2001) in their
phylogeny of the Chloridoideae based on matK sequences included Schedonnardus Steud. in a well-supported clade with
Aegopogon and Muhlenbergia. On the basis of anatomical
characters, Muhlenbergia appears to be divisible into three major groups corresponding to two subgenera, Muhlenbergia subg.
Muhlenbergia and M. subg. Trichochloa, the latter subgenus
with two sections, Muhlenbergia sect. Epicampes and M. sect.
Podosemum (Peterson 2000; Peterson and Herrera Arrieta,
2001). Analyzing ITS and trnL-trnF sequences of 52 species of
American Journal of Botany
1534
Muhlenbergia, Columbus et al. (2010) also found support
for two clades containing species of Muhlenbergia subg.
Muhlenbergia and M. subg. Trichochloa. In a large molecular
study of the entire Chloridoideae, Peterson et al. (2010) found
strong support for the five clades within 33 sampled species of
Muhlenbergiinae: Muhlenbergia subg. Muhlenbergia, M. subg.
Trichochloa, M. sect. Bealia, M. subg. Clomena, and an unnamed clade that includes three species of Chaboissaea, two
species of Lycurus, Redfieldia, Schaffnerella, Schedonnardus,
M. arenacea (Buckley) Hitchc., M. richardsonis (Trin.) Rydb.,
and M. uniflora (Muhl.) Fernald.
Using an analysis of plastid and nuclear DNA sequences, we
provide a clear phylogeny for 124 of the 176 (70%) species that
occur in the Muhlenbergiinae. We estimate the phylogeny of the
Muhlenbergiinae based on the analysis of seven molecular
markers (nuclear ITS and plastid ndhA intron, ndhF, rps16-trnK,
rps16 intron, rps3, and rpl32-trnL DNA sequences). Previously,
Columbus et al. (2010) considered 52 species of Muhlenbergia
(plus 14 additional species from the other nine Muhlenbergiinae genera) for two molecular markers (nuclear ITS and plastid
trnL-F DNA sequences). We include an expanded survey of the
Muhlenbergiinae by sampling an additional 105 species for
seven markers (687 new sequences), which is a significant advance over Peterson et al. (2010) and Columbus et al. (2010).
Our study includes 109 species of Muhlenbergia, 15 additional
species from the other nine Muhlenbergiinae genera and sequences for six plastid and ITS markers. We compare the
ITS and plastid based phylogenies with the classifications in
Columbus et al. (2010) and Peterson et al. (2001, 2007a, 2010).
In addition, we seek morphological and anatomical characters
supporting relationships in the molecular phylogenies and propose changes to the classification.
[Vol. 97
sample from a different location for the same species. All vouchers are deposited
in the Smithsonian Institution, United States National Herbarium (US). The majority of samples (89%) used in this study were collected by P. M. Peterson from
1984 to 2008. In addition, where feasible, we sampled older herbarium specimens
to maximize the number of outgroup genera in the Chloridoideae.
Molecular methods—All procedures where performed in the Laboratory of
Analytical Biology (LAB) at the Smithsonian Institution. DNA was isolated
using the BioSprint 96 DNA Plant Kit (Qiagen, Valencia, California, USA)
following the protocol of the manufacturer. PCR amplifications were performed
in MJ Research or PE 9700 thermal cyclers. Genomic DNA was combined with
1× reaction buffer (200 mM Tris-HCl, 500 mM NH4) [Bioline Biolase Taunton,
Madison, Wisconsin, USA] without Mg2+, 2 mM MgCl2, 200 mM dNTPs, 1.5
µL of Taq polymerase (Bioline Biolase Taunton), 40 pmol/µL each of forward
and reverse primers.
We targeted seven regions for sequencing: three from the plastid large single
copy (LSC) region: rps3 (coding), rps16 intron, and 3′rps16-5′trnK (spacer); three
from the small single copy (SSC) region: ndhF (coding), ndhA intron, and rpl32trnL (spacer); and nrDNA ITS. Intergenic spacers rpl32-trnL (SSC) and rps16trnK (LSC) are two of the top ranked, most variable noncoding regions for
phylogenetic studies in the angiosperms (Shaw et al., 2007). We chose the widely
used ndhF gene (SSC) to recover phylogenetic relationships because it proved
useful in other groups of grasses (Giussani et al., 2001; Soreng et al., 2007; Romaschenko et al., 2010). The sequences, melting temperature, quality, and references for the primers used are given in Peterson et al. (2010).
The amplification parameters for all plastid and the nuclear ribosome ITS
regions follow Peterson et al. (2010). All PCR products were cleaned with ExoSAP-IT (USB, Cleveland, Ohio, USA). DNA sequencing was performed with
BigDye Terminator Cycle Sequencing v.3.1 (PE Applied Biosystems, Foster
City, California, USA) according to the following parameters: 80°C, 5 min; 25 or
30 cycles of 95°C for 10 s, 50°C for 5 s and 60°C for 4 min. Sequenced products
were analyzed on an ABI PRISM 3730 DNA Analyzer 7900HT. The regions
rpl32-trnL, rps3, rps16 intron, 3′rps16-5′trnK, ndhF (coding region), and ITS
were sequenced in one direction. Relatively short regions (500–750 bp) covered
by our primers were easily interpreted allowing us to accumulate sequences from
different parts of the genome for phylogenetic inference (Shaw et al., 2005, 2007).
The ndhA intron (933 bp) was sequenced in both directions and the program Sequencher 4.8 (Gene Code Corp., Ann Arbor, Michigan, USA, 1991–2007) was
employed to produce the contig sequence for the entire region.
MATERIALS AND METHODS
Taxon sampling—Representatives of 37 genera were chosen as outgroups
from the Chloridoideae clade in Peterson et al. (2010): Aeluropus, Allolepis,
Astrebla, Austrochloris, Blepharidachne, Bouteloua, Chloris, Crypsis, Cynodon, Dasyochloa, Distichlis, Eleusine, Erioneuron, Gouinia, Gymnopogon,
Hilaria, Jouvea, Lepturus, Microchloa, Monanthochloe, Monelytrum, Mosdenia, Munroa, Orinus, Perotis, Pogonarthria, Scleropogon, Sohnsia, Sporobolus, Swallenia, Tragus, Trichoneura, Tridens, Trioidia, Vaseyochloa,
Willkommia, and Zoysia (for a complete list of species see Appendix 1).
Voucher information and GenBank numbers for 178 accessions representing
162 species are given in Appendix 1. Fifteen of the accessions included a second
Table 2.
Phylogenetic analyses—Sequence alignment was done manually using the
program BioEdit v.7.0.5.3 (Hall, 1999). Several ambiguously aligned regions
were excluded from analyses. The length of sequences and amount of excluded
data for each region is presented in Table 2. We used the maximum parsimony
analysis implemented in PAUP* to calculate the tree length (TL), consistency
index (CI), homoplasy index (HI), retention index (RI), and rescaled consistency
index (RC) for separate and combined regions (Table 2). No data were excluded
from rps3, rps16 intron, and ndhA intron. All gaps were treated as missing data.
We used maximum likelihood and Bayesian analysis to infer phylogeny. The
maximum likelihood (ML) analysis was conducted with the program GARLI
0.951 (Zwickl, 2006). Bayesian and maximum likelihood analyses yielded trees
Summary data for six plastid regions and nrDNA ITS used in this study.
Characteristic
ndhF
rpl32-trnL
rps16-trnK
rps3
rps16 intron
ndhA intron
Plastid
ITS
Aligned sequence length
Average sequence length
No. of taxa
No. of excluded characters
Proportion of excluded characters (%)
No. of PIC
PIC/SL
Tree length
Consistency index
Homoplasy index
Retention index
Rescaled consistency index
Akaike information criterion
796
734
163
2
0.3
169
0.230
569
0.4271
0.5729
0.8344
0.3564
GTR+G
1389
695
175
364
26.2
258
0.371
761
0.5361
0.4639
0.8450
0.4530
TVM+G
1222
723
174
213
17.4
221
0.306
575
0.5513
0.4487
0.8428
0.4646
TVMef+G
590
579
174
0
0.0
85
0.147
254
0.4764
0.5236
0.8679
0.4135
TVM+G
1368
745
165
0
0.0
159
0.213
400
0.5800
0.4200
0.8768
0.5086
K81uf+G
1424
933
161
0
0.0
256
0.274
708
0.5508
0.4492
0.8674
0.4778
K81uf
6789
4409
177
579
8.5
1148
0.260
3369
0.508
0.492
0.844
0.429
GTR+G
814
669
172
89
10.9
312
0.466
2373
0.284
0.716
0.689
0.196
GTR+G
Notes: PIC, parsimony informative characters; SL = sequence length
Combined
plastid+ITS
7603
5078
179
743
9.8
1460
0.288
5859
0.407
0.593
0.784
0.319
GTR+G
September 2010]
Peterson et al.—Phylogeny of Muhlenberginiinae
with visually similar topology, i.e., the trees are visually the same, but some
branch lengths could differ minutely. A test run of Bayesian analysis for the combined data sets under the single GTR+G model yielded the same topology and
posterior probability (PP) values as the Bayesian analysis for a partitioned data set
performed under models suggested by MODELTEST for separate regions.
The Akaike information criterion (AIC) scores are indicated in Table 2
(Kimura, 1981; Tavaré, 1986; Posada and Crandall, 1998). Very little conflict was
observed among maximum likelihood trees in the individual plastid analyses. The
incongruence length difference (ILD) test (Farris et al., 1994) was implemented
in the program WinClada ver. 1.00.08 (Nixon, 2002) to test for incongruence
between the ITS and plastid data sets. Default parameters for 1000 replicates were
executed.
Bootstrap analyses (Felsenstein, 1985) were performed for the ML analysis
using GARLI with the default parameters for 1000 replicates, with the program
PAUP* ver. 4.0b10 (Swofford, 2000) used to compute the bootstrap consensus
tree. Bootstrap (BS) values of 90–100% were interpreted as strong support,
70–89% as moderate, and 50–69% as weak.
Bayesian posterior probabilities were estimated using the program MRBAYES
ver. 3.01 (Huelsenbeck and Ronquist, 2001; Ronquist et al., 2005) with DNA
substitution models selected using the program MrModeltest ver. 1.1b (Nylander,
2002). The plastid data set and combined plastid+ITS data set for Bayesian analysis were then partitioned into two subsets that were processed implementing different parameters suggested by MrModeltest concerning the model for among site
rate variation, number of substitution types, substitution rates, and gamma shape
parameter. All other parameters were left at default settings. Each Bayesian analysis was initiated with random starting trees and was initially run for 2 million
generations, sampling once per 100 generations. The analysis was continued until
the value of standard deviation of split sequences dropped below 0.01 as the convergence diagnostic value (Huelsenbeck and Ronquist, 2001). The fraction of the
sampled values discarded as burn in was set at 0.25.
RESULTS
Phylogenetic analyses— A total of 687 sequences representing 105 species are newly reported in GenBank (Appendix 1).
Lengths sequenced for individual regions are noted in Table 2.
Plastid rpl32-trnL had the highest rate of amplification and successful sequencing with 99% of taxa recovered across the entire
data set. Recovery in other plastid regions ranged from 91–98%,
and the effectiveness of sequencing the ITS region was 97%
(Table 2). An average of 4.5% of data was missing across the
entire data set. As expected, ITS provided the most information
per aligned nucleotide (Table 2; the ratio of the number of parsimony informative characters (PIC) per sequence length (SL)
was 0.466, compared with 0.147–0.371 for plastid regions).
Analysis of ITS sequences— There are five major clades
within a monophyletic Muhlenbergiinae (moderate support),
labeled in Fig. 1 as Muhlenbergia sect. Bealia (strong support),
M. subg. Trichochloa (strong support), M. subg. Clomena
(moderate support), M. sect. Pseudosporobolus (weak support),
and M. subg. Muhlenbergia (moderate support). Muhlenbergia
sect. Bealia and subg. Trichochloa share a common ancestor
(strong support), and M. subg. Clomena and sect. Pseudosporobolus form a clade (moderate support) that is sister to
M. subg. Muhlenbergia (strong support). Muhlenbergia ramulosa is sister to the rest of the Muhlenbergiinae.
Muhlenbergia sect. Bealia consists of 20 taxa and contains
strongly supported clades of M. caxamarcensis and M. filiformis;
two accessions of Blepharoneuron shepherdii; M. argentea, M.
eludens, and M. flavida; M. arenicola and M. torreyi, which are
sister to eight annual species; and M. minutissima and M. sinuosa. There are 42 taxa included within M. subg. Trichochloa
clade (six of these have two samples per species) and these
show very little sequence divergence because all branches are
very short. A single clade exhibits strong support for two acces-
1535
sions of M. lucida. Muhlenbergia subg. Clomena contains 11
taxa (two of these have two samples per species) divided into
two well-supported clades: M. durangensis-M. flaviseta sister
to the remaining species. Muhlenbergia sect. Pseudosporobolus consists of 22 taxa (three of these have two samples per
species) and contains strongly supported clades comprising
M. implicata and M. jaime-hintoni; two different accessions of
M. uniflora; M. fastigiata sister to two accessions of M. richardsonis; two different accessions of Lycurus setosus; and
Chaboissaea subbiflora, C. atacamensis, and C. ligulata. There
are 38 taxa within M. subg. Muhlenbergia (two of these have
two samples per species) with seven well-supported clades:
M. spiciformis and M. tenuifolia; M. appressa, M. brandegei,
and M. microsperma; Pereilema beyrichianum and P. crinitum;
M. ciliata, M. pectinata, and M. tenella; Aegopogon cenchroides and A. tenellus; M. andina, M. curtifolia, and M. thurberi;
and M. sobolifera and M. tenuiflora.
Analysis of plastid sequences— As in the ITS tree, five major clades appear to be within a monophyletic Muhlenbergiinae
(strongly supported), and these are labeled in Fig. 2 as Muhlenbergia sect. Bealia (weakly supported), M. subg. Trichochloa
(moderately supported), M. subg. Clomena (moderately supported), M. sect. Pseudosporobolus (weakly supported), and M.
subg. Muhlenbergia (strongly supported). Species composition
in each of these five clades is identical with the ITS-derived
phylogram, except for the five additional taxa included in the
data set. As in the ITS-derived phylogram, Muhlenbergia sect.
Bealia and subg. Trichochloa share a common ancestor (strongly
supported), and M. subg. Clomena and sect. Pseudosporobolus
form a clade (moderately supported) that is sister to M. subg.
Muhlenbergia (moderately supported. Muhlenbergia ramulosa
is sister to M. sect. Bealia and M. subg. Trichochloa (strongly
supported).
There is considerably higher backbone support among clades
within Muhlenbergia sect. Bealia, and there is one additional
taxon not included in the ITS data set, M. vaginata, that forms
a clade with M. filiformis (strongly supported); sister to this is
M. caxamarcenis (strongly supported). Other strongly supported
clades in M. sect. Bealia include M. arizonica-M. argenteaM. eludens-M. flavida, two species of Blepharoneuron with two
accessions of B. shepherdii, and two clades that are sister:
((M. minutissima, M. texana)(M. sinuosa (M. brevis, M. depauperata))) and ((M. arenicola, M. torreyi)(M. fragilis (M. annua,
M. majalcensis))).
Muhlenbergia subg. Trichochloa contains more internal support as compared to the ITS-derived phylogeny with strong
support for separate clades containing M. elongata, M. emersleyi,
and M. lucida; and M. involuta, M. reverchonii, and M. sericea.
The two accessions each of M. dubia, M. lucida, M. pubescens,
and M. rigida do not form sister groups. In the M. subg. Clomena clade, Muhlenbergia filiculmis, M. jonesii, two accessions
of M. montana and M. virescens, M. quadridentata and M.
straminea form a well-supported clade; sister to this are M.
crispiseta-M. peruviana pair (strongly supported). As in the
ITS-derived phylogeny, M. durangensis-M. flavida pair
(strongly supported) is sister to the remaining species in M.
subg. Clomena.
Backbone support for M. sect. Pseudosporobolus is much
higher in the plastid-derived phylogram, and the topology is
somewhat different than in the ITS tree. Strongly supported
clades include two accessions of Lycurus setosus, M. palmirensis-M. villiflora var. villosa, Chaboissaea subbiflora sister
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[Vol. 97
Fig. 1. Phylogram of best maximum likelihood tree from analysis of nuclear ITS data. Numbers above branches represent bootstrap values; numbers
below branches are posterior probability values. (A) Detail of upper portion and (B) lower portion of phylogram. Abbreviations for subtribes: A = Aeluropodinae,
B = Boutelouinae, E = Eleusininae, H = Hilariinae, Mo = Monanthochloinae, Sc = Scleropogoninae, Td = Triodinae, Tg = Traginae, Tt = Tridentinae. Taxon
color indicates native distribution: green = North America, blue = South America, purple = North and South America, red = southeast Asia.
September 2010]
Peterson et al.—Phylogeny of Muhlenberginiinae
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American Journal of Botany
to C. atacamensis-C. ligulata, Redfieldia flexuosa sister to two
accessions of M. uniflora, M. fastigiata sister to M. repens-M.
utilis with these three sister to two accessions of M. richardsonis. One other large clade with strong support includes Schedonnardus paniculatus as sister to a clade of (in phylogenetic
order) three species of Chaboissaea, M. cuspidata, M. palmirensis-M. villiflora var. villosa, M. wrightii, Schaffnerella gracilis, and two accessions of Lycurus setosus. Muhlenbergia
jaime-hintoni is sister to Redfieldia flexuosa-M. uniflora (Fig.
2B) rather than to M. implicata in the ITS tree (Fig. 1B).
The topology of the plastid-derived phylogram for M. subg.
Muhlenbergia is similar to that portrayed by the ITS-derived
phylogram, although many branches have higher support values and the topology of a few clades is different. A derived,
moderately supported clade with all species occurring in southeast Asia includes M. ramosa sister (strongly supported) to two
accessions of M. japonica (moderately supported) and M. himalayensis-M. huegelii (strongly supported). Other strongly
supported clades includeM. racemosa-M. tenuiflora (in the ITS
tree, M. tenuiflora forms a strongly supported clade with M.
sobolifera), M. andina sister to M. curtifolia-M. thurberi, M.
pauciflora and M. glauca 21023 (there are two different accessions for this species, see Appendix 1) -M. polycaulis, Pereilema
beyrichianum-P. crinitum, M. breviseta-M. dumosa, M. alamosae sister to M. tarahumara that is sister to Aegopogon cenchroides-A. tenellus, M. arsenei (in the ITS tree, M. arsenei is sister
to Pereilema crinitum-P. beyrichianum) sister to M. tenella
-M. ciliata-M. pectinata, M. spiciformis-M. tenuifolia sister to
M. porteri that is sister to M. appressa-M. brandegei-M. microsperma. Muhlenbergia mexicana var. filiformis is a moderately supported sister to clade (M. sobolifera (M. californica
(M. racemosa, M. tenuiflora))), whereas in the ITS tree it
is sister to M. californica in a larger clade, ((M. sobolifera,
M. tenuiflora)(M. racemosa (M. californica, M. mexicana var.
filiformis))).
Analysis of combined plastid and ITS sequences— The ILD
test (P = 0.1667; 99% confidence level) failed to reject the null
hypothesis of congruence between the ITS and plastid data sets;
therefore, we combined them. As in the ITS and combined plastid trees, five major clades seem to be within a monophyletic
Muhlenbergiinae (strongly supported), and these are labeled in
Fig. 3 as Muhlenbergia sect. Bealia (strongly supported), M.
subg. Trichochloa (strongly supported), M. subg. Clomena
(moderately supported), M. sect. Pseudosporobolus (moderately supported), and M. subg. Muhlenbergia (strongly supported). Species composition in each of these five clades is
again identical with the ITS and plastid-derived phylograms.
As in the other analyses, Muhlenbergia sect. Bealia and subg.
Trichochloa share a common ancestor (strongly supported),
and M. subg. Clomena and sect. Pseudosporobolus form a clade
(strongly supported) that is sister to M. subg. Muhlenbergia
(strongly supported). Muhlenbergia ramulosa is sister to
M. sect. Bealia and M. subg. Trichochloa as in the ITS-derived
phylogram.
The overall topology of the combined phylogram is remarkably similar to that of the plastid-derived tree, even in the terminal branches. There are only some minor differences with the
plastid phylogeny, most notably in M. sect. Pseudosporobolus
where M. fastigiata is sister (strongly supported) to two accessions of M. richardsonis and in M. subg. Muhlenbergia where
M. sobolifera-M. tenuiflora form a clade (strongly supported)
that is sister (strongly supported) to M. racemosa, M. californica,
[Vol. 97
and M. mexicana var. filiformis. However, these relationships
were depicted in the ITS-derived phylogram. Therefore, in the
following sections we will refer to the combined plastid ITSderived phylogram when discussing evolutionary scenarios. In
the discussion section, we make all necessary combinations and
new names within Muhlenbergia.
Analysis of outgroups— Determination of the sister to the
Muhlenbergiinae allows us to test the monophyly of the subtribe and to polarize morphological and anatomical characters.
The ITS and plastid trees differed in relative branch length, support values that occur on these branches, and topology among
the 38 taxa used as outgroups. In the ITS phylogram (Fig. 1) the
sister to the Muhlenbergiinae was a clade (PP = 0.75) containing Sohnsis filifolia as sister to the Scleropogoninae. In the plastid and combined ITS/plastid tree (Figs. 2, 3), Sohnsia filifolia
was sister to the Muhlenbergiinae, and the Scleropogoninae
was the sister group to both of these. Relative positions of Swallenia, Tragus, and Jouvea differ among the ITS, plastid, and
combined ITS/plastid phylograms. Relationships among these
three taxa in the tribe Cynodonteae have been thoroughly investigated by Peterson et al. (2010) using a much broader sample.
DISCUSSION
Monophyly of the Muhlenbergiinae is moderately to strongly
supported by our data in all trees and Muhlenbergia, as traditionally treated by agrostologists, is depicted as paraphyletic
with Aegopogon, Bealia, Blepharoneuron, Chaboissaea, Lycurus, Pereilema, Redfieldia, Schaffnerella, and Schedonnardus
embedded within this clade (Duvall et al., 1994; Hilu and Alice,
2001; Columbus et al., 2007, 2010; Peterson et al., 2010). Because the monophyly of Muhlenbergia s.s. or s.l. is not supported by phylogenetic analysis of ITS, matK, ndhA intron,
ndhF, rps16-trnK, rps16 intron, rps3, and rpl32-trnL, trnL-trnF
sequences, and RFLP studies (Duvall et al., 1994; Hilu and
Alice, 2001; Columbus et al., 2007, 2010; Peterson et al., 2010),
we are incorporating all nine genera within Muhlenbergia.
Within the Muhlenbergia clade (=Muhlenbergiinae) there are
five large, well-supported clades: Muhlenbergia sect. Bealia,
M. subg. Trichochloa, M. subg. Clomena, M. sect. Pseudosporobolus, and M. subg. Muhlenbergia.
The M. subg. Muhlenbergia clade includes only species that
exhibit PCK-like leaf anatomical characteristics, where the
chlorenchyma is composed of tabular cells that are indistinctly
radiate and continuous between bundles [PCK type, defined as
centrifugal/evenly distributed photosynthetic carbon reduction
(PCRD) cell chloroplasts (with grana), the major veins (which,
at maturity have a protoxylem lacuna and large metaxylem elements) are surrounded by two bundle sheaths, an inner mestome sheath of elongate nonchlorenchymatous cells and an
outer chlorenchymatous sheath of shorter PCRD cells (designated XyMS+structural type; Hattersley and Watson, 1976,
1992; Dengler et al., 1986) with suberized lamella, fan- to
shield-shaped bulliform cells without formation of a complete
column of colorless cells from the adaxial to the abaxial surface, and species that have four or more secondary and/or tertiary vascular bundles between consecutive primary vascular
bundles (Peterson and Herrera Arrieta, 2001). Morphologically,
members of the M. subg. Muhlenbergia clade have broad, flat
leaf blades, most have well-developed, scaly, and creeping
rhizomes, and panicles that are usually narrow at maturity
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Peterson et al.—Phylogeny of Muhlenberginiinae
(M. porteri is an exception with open, 6–15 cm wide panicles)
(Peterson, 2003). Our study supports a previous hypothesis of
Peterson and Herrera Arrieta (2001) that within Muhlenbergia
the evolution of the PCK subtype of photosynthesis was a single evolutionary event. Early in the evolution of Muhlenbergia,
the PCK-like condition appears to have arisen once, because all
species that have been chemically assayed as PCK occur in this
clade (Gutierrez et al., 1974; Brown, 1977). Ecologically,
Muhlenbergia PCK-like species are able to flourish in shaded
sites and forest margins with low-light intensities and moisthumid microhabitats that are not normally occupied by their
NAD-ME relatives.
In our ITS phylogram within the M. subg. Muhlenbergia
clade, species of Pereilema do not appear monophyletic because they form a poorly supported grade (BS = 67, PP = 0.97),
and P. ciliatum is paired with M. flexuosa (unsupported). In our
plastid and combined phylogram, all species of Pereilema form
a weak to moderately supported clade. Because it would require
quite a few parallel evolutionary events to select for the morphological features expressed in this genus, our plastid markers
may be a better estimate of phylogeny in this lineage. All four
species of Pereilema have two unique characters: sterile, bristle-like spikelets that subtend the fertile spikelets and prominent
blade auricles that are usually ciliate (Peterson, 2000).
Embedded with M. subg. Muhlenbergia is a strongly supported clade containing Aegopogon cenchroides and A. tenellus.
The four species of Aegopogon have a false spike with each
branch usually bearing three spikelets with one larger spikelet
perfect and the other two smaller and often staminate or rudimentary (two spikelets in A. bryophilus Döll with one spikelet
often not developed) (Peterson, 2000). The recently described
species M. tarahumara (Peterson and Columbus, 2009) was
found in our study to be sister to Aegopogon in all trees. Muhlenbergia tarahumara differs from other species of Aegopogon by
having panicle branches with only two terminal, perfect spikelets (Peterson and Columbus, 2009). Anatomically, M. tarahumara also differs from other species in M. subg. Muhlenbergia
by having noncontiguous chlorenchyma separated by columns
of colorless cells between adjacent vascular bundles. Other species in this clade (M. pauciflora and M. polycaulis) exhibit this
leaf anatomical characteristic, at least near the middle of the
blades. However, near the leaf margins, the tertiary vascular
bundles of these latter two species have chlorenchyma tissue
that is continuous between each adjacent vascular bundle. All
other characteristics, i.e., presence of two bundle sheaths, uneven outline of the outer sheath, round shape of chloroplasts in
the outer sheath, and centrifugal/peripheral position of the chloroplasts in each cell, are predictive of PCK for M. pauciflora,
M. polycaulis, and M. tarahumara. Because the habitat where
M. tarahumara is found is rather xeric (slopes, ridge tops, rock
outcrops), the columns of colorless cells between adjacent vascular bundles, like most NAD-ME species, facilitate involution
of the leaf blades, an adaption to periods of drought. PCK-like
leaf anatomy appears to have arisen once in the evolution of the
Muhlenbergiinae, and this morphology is linked to species that occupy slightly more mesic habitats (Peterson and Herrera Arrieta,
2001). The anatomical structure found in M. tarahumara, and
to some extent in M. pauciflora and M. polycaulis, might be in
direct response to the environment where reversion to NAD-MElike leaf structure is likely an adaptive feature.
The Chinese species M. himalayensis, M. hueglii, M. japonica, and M. ramosa form a clade within M. subg. Muhlenbergia
with moderate bootstrap support in the plastid and combined
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plastid/ITS phylograms, suggesting a single colonization event,
most likely from North American origins. Only seven native
species of Muhlenbergia occur in southeast Asia, and all seven
are reported in the flora of China (Wu and Peterson, 2006). The
Asian species of Muhlenbergia are predominately rhizomatous
(only M. duthieana Hack. is loosely caespitose without rhizomes) and occur in similar habitats to most species in M. subg.
Muhlenbergia, such as mountain slopes, forests, and along
moist roadsides. Muhlenbergia californica, M. mexicana var.
filiformis, M. racemosa, M. schreberi, M. sobolifera, and M.
tenuiflora are sister to these Chinese species, and together they
are sister to the remaining species within M. subg. Muhlenbergia,
suggesting that colonization from North America to southeastern
Asia occurred relatively recently in the evolution of this subgenus
(Figs. 1–3).
Three sections of Muhlenbergia recognized by Pilger (1956):
sect. Acroxis (M. dumosa, M. mexicana, M. polycaulis, and M.
racemosa), sect. Muhlenbergia (M. schreberi), and sect. Stenocladium (M. bushii R. W. Pohl, M. hueglii, M. japonica, M.
ramosa, M. sobolifera, and M. tenuiflora) included species in
our subg. Muhlenbergia clade. In our phylograms, there are no
clades that correspond with Pilger’s sections; therefore, we
agree with earlier authors that his treatment was not phylogenetically informative (Soderstrom, 1967; Pohl, 1969; Morden,
1985; Peterson and Annable, 1991).
Although the clade of species representing the M. subg.
Trichochloa is strongly supported in our analyses (Figs. 1, 3),
there is little resolution among members, likely reflecting very
low levels of divergence within our plastid and nrDNA ITS sequences. The low level of divergence may be a consequence of
rapid speciation events. It is possible that some species delimitations of subg. Trichochloa are not tenable because of recent
diversification although it may also be the case that suitable
molecular markers have yet to be applied. Within Muhlenbergia, this group is by far the most difficult to determine because
there are very few morphological differences among the taxa
and discrete (nonplastic) characteristics are few. Anatomically,
most species in this clade have sclerosed phloem, a crown of
inflated cells located adaxially to the primary vascular bundles,
unequal secondary and tertiary vascular bundles, and primary
vascular bundles that are either rectangular or obovate/elliptic
in shape (Peterson and Herrera Arrieta, 2001). Species in M.
subg. Trichochloa are erect, relatively tall (0.8–3 m), robust and
stout, caespitose perennials that have unnerved or 1-nerved
glumes (Soderstrom, 1967; Peterson, 2000). Pilger (1956) recognized M. sect. Cinnastrum with narrowly contracted, spicate
panicles (M. angustata, M. macroura, and M. rigens) and M. sect.
Podosemum with open panicles, lemmas long aristate, new
shoots inside the sheaths (intravaginal), and ligule extended
(M. articulata, M. capillaris, M. distichophylla, M. longiglumis, M. rigida, and M. stricta). Pilger’s two sections do not include the same species as M. subg. Trichochloa sects. Epicampes
and Podosemum as described in Peterson and Herrera Arrieta
(2001), but the species treated by Soderstrom (1967) in his
subg. Podosemum (=M. subg. Trichochloa) are the same.
The clade of M. subg. Clomena (=M. montana complex sensu
Herrera Arrieta, 1998) is moderately supported in our analysis,
and morphologically, this complex includes species that have
3-nerved upper glumes that are often 3-toothed and densely
caespitose individuals with lower leaf sheaths that become flat
and somewhat papery at maturity (Reeder and Reeder, 1995;
Herrera Arrieta, 1998). Muhlenbergia argentea, a species with
1-nerved upper glumes, slightly compressed-keeled sheaths,
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[Vol. 97
Fig. 2. Phylogram of best maximum likelihood tree from analysis of plastid data. Numbers above branches represent bootstrap values; numbers below
branches are posterior probability values. (A) Detail of upper portion and (B) lower portion of phylogram. Abbreviations for subtribes: A = Aeluropodinae,
B = Boutelouinae, E = Eleusininae, H = Hilariinae, Mo = Monanthochloinae, Sc = Scleropogoninae, Td = Triodinae, Tg = Traginae, Tt = Tridentinae. Taxon
color indicates native distribution: green = North America, blue = South America, purple = North and South America, red = southeast Asia.
September 2010]
Peterson et al.—Phylogeny of Muhlenberginiinae
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American Journal of Botany
and flattened caryopses (Reeder and Reeder, 1995) was included by Herrera Arrieta (1998) in her study of the M. montana
complex; however, this taxon occurs in our clade of M. subg.
Bealia. We provide evidence for the exclusion of M. argentea
and the addition of two annual species, M. crispiseta and
M. peruviana (Peterson and Annable, 1991) to be included in
M. subg. Clomena. Within our clade of M. subg. Clomena, there
are three strongly supported subclades, one that includes the
two annual species, a second that includes M. durangensis and
M. flaviseta, and a third that includes those species with morphologies very similar to M. montana. Some individuals of M.
montana and M. virescens have sclerosed phloem. This characteristic apparently has arisen four times within Muhlenbergia
because it also is found in subg. Trichochloa, in M. arenicola
and M. torreyi (subg. Bealia), and in M. jaime-hintoni (sect.
Pseudosporobolus) (Peterson and Herrera Arrieta, 2001).
The moderately supported clade of M. sect. Pseudosporobolus (Fig. 3) includes a diverse assemblage of species, such as
Schedonnardus paniculatus, that has panicles with long primary branches that do not rebranch, hence containing nearly
sessile spikelets; Redfieldia flexuosa with 2–6-flowered spikelets, a line of hairs for a ligule, and open and diffuse panicles
with capillary branches very similar to M. asperifolia, also occasionally with 2- or 3-flowered spikelets; Schaffnerella gracilis,
a little known endemic of San Luis Potosí, Mexico (Columbus
et al., 2002) that has panicles composed of short primary
branches, each bearing a triad of 1-flowered spikelets, 7–9-nerved
lemmas that have 3–5 awns, all enclosed in a spathiform sheath;
Lycurus setosus with spikelets that are grouped in pairs, one
sessile and one pedicellate; and Chaboissaea with one or two
(occasionally three) florets per spikelet, the lower floret perfect
and the upper florets staminate or sterile (Reeder, 1985; Sánchez
and Rúgolo de Agrasar, 1986; Peterson and Annable, 1992;
Peterson 2000; Peterson et al., 2007b). Embedded in M. sect.
Pseudosporobolus is a strongly supported clade (Fig. 3)
consisting of M. fastigiata, M. repens, M. richardsonis, and
M. utilis, all earlier treated as the M. repens complex (Morden,
1985; Morden and Hatch, 1987, 1996). These four species are
characterized by having short culms seldom exceeding 40 cm in
height; a rhizomatous perennial habit, short involute leaf blades;
short, narrow, contracted panicles; plumbeous spikelets; and
unawned or mucronate lemmas (Morden, 1985; Morden and
Hatch, 1987, 1996). Muhlenbergia villiflora var. villosa was included in Morden’s M. repens complex, but in our analyses, it
is sister to the Ecuadorian endemic M. palmirensis (Fig. 3,
moderately supported; Fig. 2, strongly supported). Most species in M. sect. Pseudosporobolus have well-developed abaxial
and adaxial sclerenchyma in their primary vascular bundles,
narrow panicles, usually plumbeous spikelets, and unawned to
mucronate lemmas (Peterson and Herrera Arrieta, 2001). Exceptions to these general trends include the short-awned Lycurus setosus and long-awned M. implicata, and the broad and
open-panicled M. asperifolia, M. implicata, and Redfieldia flexuosa. The characteristic of having 2–3(–6)-flowered spikelets is
also quite common in M. sect. Pseudosporobolus because it is
found in Chaboissaea atacamensis, C. ligulata, C. subbiflora,
M. arenacea, M. asperifolia, M. cuspidata, M. fastigiata, M.
richardsonis, M. uniflora, and Redfieldia flexuosa.
The strongly supported clade of M. sect. Bealia contains few
unique morphological characteristics shared among its members. However, all species in this clade have lemmas with hairy
margins and midveins and caespitose or tufted culms, characters that are shared by many species in the M. subg. Trichochloa
[Vol. 97
and subg. Clomena. Of the 20 species in M. sect Bealia, 14 are
annual, with only Blepharoneuron tricholepis, M. arenicola,
M. argentea, M. arizonica, M. caxamarcensis, and M. torreyi
being perennial. Blepharoneuron was originally erected by
Nash (1898) to emphasize the densely pilose margins and midvein of the lemma found in B. tricholepis. Blepharoneuron
shepherdii also has densely pilose margins and midvein of the
lemma and a base chromosome number of x = 8, prompting
Peterson and Annable (1990) to place Muhlenbergia shepherdii
(Vasey) Swallen in Blepharoneuron. The overall morphology
of B. shepherdii with species in the M. fragilis-M. annuaM. majalcensis clade (Fig. 3, moderately supported) and the
M. minutissima-M. sinuosa pair (Fig. 3, moderately supported)
is striking because all are slender annuals with unawned lemmas, with capillary, flexuous pedicels that are often nodding
(Peterson and Annable, 1990, 1991). Sister to the Blepharoneuron
pair is a strongly supported clade comprising M. caxamarcensis,
M. filiformis, and M. vaginata (Fig. 3). With the inclusion of M.
ligularis (Columbus et al., 2010), these latter four taxa form a
tight assemblage of short-lived perennial to annual, mat-forming
species with short culms not exceeding 35 cm in height, narrow
to loosely contracted panicles, and unawned, mucronate or shortawned lemmas (Laegaard and Sánchez Vega, 1990; Peterson and
Annable, 1991). Morphologically, these four species closely
resemble the M. repens complex (M. sect. Pseudosporobolus)
as previously discussed, but differ primarily by lacking welldeveloped rhizomes, a characteristic common in M. subg.
Muhlenbergia and M. arenacea, M. asperifolia, M. jaime-hintonii, M. palmirensis, M. villiflora var. villosa, and Redfieldia
flexuosa, all members of M. sect. Pseudosporobolus.
In our study, M. ramulosa does not align within any subgenus
or section but is sister to all Muhlenbergiinae in the ITS phylogram (not well supported in Fig. 1) or sister to M. sect. Bealia
and M. subg. Trichochloa in the plastid and combined phylograms (strongly supported in Figs. 2 and 3). Earlier molecular
studies of the Muhlenbergiinae (ITS and trnL-F) are also
unable to confirm the affinity of M. ramulosa (Columbus et al.,
2010), clearly a distinctive taxon, phylogenetically, wherever it
belongs. Morphologically, M. ramulosa is very similar to many
of the small delicate annuals that reside in M. sect. Bealia. At
this time, we are not prepared to erect a subgeneric ranking to
accommodate only M. ramulosa.
Cleistogamous spikelets appear to have evolved twice within
the Muhlenbergiinae, once in the M. subg. Muhlenbergia where
M. appressa, M. brandegei, and M. microsperma (all annuals)
form a strongly supported clade (Fig. 3) and in M. sect. Pseudosporobolus known only from a few collections of M. cuspidata (Morden and Hatch, 1984). The formation of cleistogamous
spikelets could actually be more common among the Muhlenbergiinae, but is undocumented to date.
Sclerosed phloem appears to have evolved a minimum of
four times within the Muhlenbergiinae because it is found in M.
arenicola-M. torreyi clade in sect. Bealia, the subg. Trichochloa
clade, the subg. Clomena clade, and in M. jaime-hintonii (sect.
Pseudosporobolus). In a cladogram derived entirely on the
analysis of 16 anatomical characters within Muhlenbergia,
Peterson and Herrera-Arrieta (2001) indicated that sclerosed
phloem originated twice.
Biogeography— All three phylograms suggest that the
Muhlenbergiinae originated in North America; for example, the
sister group (Scleropogoninae in Fig. 1; or Sohnsia filifolia and
Scleropogoninae in Figs. 2 and 3) are predominantly North
September 2010]
Peterson et al.—Phylogeny of Muhlenberginiinae
American species. The phylogenetic arrangement of the various
tribes, subtribes, and genera in our analysis is similar to that
found in Peterson et al. (2010) in which the Zoysieae is sister to
the Cynodonteae, and within the Cynodonteae nested clades of
the Aeluropodinae and Triodiinae are first, followed by the Orcuttiinae (not included), Tridentinae, Eleusininae, Tripogoninae
(not included), Pappophorinae (not included), Traginae, an
almost entirely New World clade with the Allolepis-JouveaHilariinae sister to the Monanthochloinae-Scleropogoninae,
Sohnsia filifolia, Lepturidium insulare Hitchc. & Ekman (not
included), and the remaining Muhlenbergiinae. Within the
Muhlenbergiinae, multiple independent radiations to South
America have occurred one or more times in each of the three
subgenera and two sections (blue and purple taxa in Figs. 1–3), and
15 species occur in both North and South America. The study of
amphitropical disjunctions within the Muhlenbergiinae has indicated a North American origin and recent introduction into South
America for at least three species (Peterson and Herrera Arrieta,
1995; Sykes et al., 1997; Peterson and Morrone, 1998; Peterson
and Ortíz Diaz, 1998; Peterson et al., 2007a). Other plant groups
with similar desert, amphitropical disjunct distributions have
all been postulated to be of recent origin, i.e., late Pliocene to
Pleistocene (Raven, 1963; Wen and Ickert-Bond, 2009).
Within M. subg. Muhlenbergia, there is evidence for a single
colonization event in southeastern Asia (red taxa in Figs. 1–3).
Intercontinental disjunctions between eastern North America
and eastern Asia have been investigated in insects (von Dohlen
et al., 2002) and plants (Wen, 1999, 2001; Wen et al., 2002).
This floristic disjunction has resulted from fragmentation and
range restriction of a widespread mesophytic forest during the
past that attained its intercontinental distribution via the Bering
and North Atlantic land bridges (e.g., Manchester, 1999; reviewed in Wen, 1999, 2001). Because the Asian Muhlenbergia
clade is deeply nested, it seems likely that these species attained
their current distribution recently, at least post Pleistocene.
Estimates of introduction dates will be the topic of a forthcoming biogeographic study with the use of additional markers and
a more complete sample of the species in the subtribe.
Taxonomy— Because our molecular analysis renders
Muhlenbergia paraphyletic, we propose incorporating Aegopogon, Bealia, Blepharoneuron, Chaboissaea, Lycurus, Pereilema,
Redfieldia, Schaffnerella, and Schedonnardus within Muhlenbergia. Muhlenbergia is the oldest name. Expansion of the circumscription to include these nine genera within Muhlenbergia
requires the least amount of nomenclatural changes and still
allows us to recognize a strongly supported monophyletic and
morphologically cohesive unit. A complete classification for
the Chloridoideae of the New World can be found in Soreng et
al. (2009), and an attempt to place most genera within the subfamily into the four recognized tribes is found in Peterson et al.
(2010). Below, we list all species in these nine genera and provide their name in Muhlenbergia. Our analysis also supports
the recognition of five major clades within Muhlenbergia, and
for consistency in rank, we propose two new subgeneric combinations below.
Muhlenbergia alopecuroides (Griseb.) P. M. Peterson &
Columbus, Madroño 55(2): 159. 2008. Basionym: Lycurus
alopecuroides Griseb., Abh. Königl. Ges. Wiss. Göttingen 19:
255–256. 1874. Heterotypic synonym: Pleopogon setosum
Nutt., Proc. Acad. Nat. Sci. Philadelphia 4: 25. 1848. Lycurus
setosus (Nutt.) C. Reeder, Phytologia 57: 287. 1985. non
Muhlenbergia setosa (Kunth) Trin.
1543
Muhlenbergia ammophila P. M. Peterson, nom. nov. Replaced
name: Graphephorum flexuosum Thurb. ex A. Gray, Proc.
Acad. Nat. Sci. Philadelphia 1863: 78. 1864. Redfieldia flexuosa
(Thurb. ex A. Gray) Vasey, Bull. Torrey Bot. Club 14: 133.
1887. non Muhlenbergia flexuosa Hitchc. Notes: The species is
usually found growing on sand hills and dunes; therefore, it
seems appropriate to emphasize its habitat requirement by using
the epithet “ammophila” or sand loving.
Muhlenbergia atacamensis Parodi, Revista Argent. Agron.
15: 248. 1948. Chaboissaea atacamensis (Parodi) P. M. Peterson
& Annable, Madroño 39(1): 19. 1992.
Muhlenbergia subg. Bealia (Scribn.) P. M. Peterson, comb.
stat. nov. Basionym: Bealia Scribn., The True Grasses 104, f. 45a.
1890. Muhlenbergia sect. Bealia (Scribn.) Pilg., Die Natülichen
Planzenfamilien, Zweite Auflage 14d: 71. 1956.
Muhlenbergia beyrichianum Kunth, Enum. Pl. 1: 200. 1833.
Pereilema beyrichianum (Kunth) Hitchc., Contr. U. S. Natl.
Herb. 24(8): 385. 1927.
Muhlenbergia biloba Hitchc., Contr. U. S. Natl. Herb. 17(3):
294. 1913. Replaced name: Bealia mexicana Scribn., The True
Grasses 103, f. 45a. 1890. non Muhlenbergia mexicana (L.)
Trin., Gram. Unifl. Sesquifl. 189, 190, 297, t. 5, f. 8. 1824.
Muhlenbergia bryophilus (Döll) P. M. Peterson, Caldasia
31(2): 279. 2009. Basionym: Aegopogon bryophilus Döll, Fl.
Bras. 2(3): 239. 1880.
Muhlenbergia cenchroides (Humb. & Bonpl. ex Willd.) P. M.
Peterson, Caldasia 31(2): 280. 2009. Basionym: Aegopogon
cenchroides Humb. & Bonpl. ex Willd., Sp. Pl. 4(2): 899. 1806.
Muhlenbergia columbi P. M. Peterson, nom. nov. Replaced
name: Schaffnera gracilis Benth., Hooker’s Icon. Pl. 14: 59. T.
1378. 1882. later near hom., non Schaffneria Moore (1857). non
Muhlenbergia gracilis (Kunth) Trin. Schaffnerella gracilis
(Benth.) Nash, N. Amer. Fl. 17(2): 141. 1912. Notes: The specific epithet commemorates J. Travis Columbus who led a trip to
San Luis Potosí, Mexico and was the first to collect this enigmatic
species again more than 120 yr after the original collections by
J. G. Schaffner between 1876 and 1880 (Columbus et al., 2002).
Muhlenbergia decumbens Swallen, Bol. Soc. Bot. Mexico 23:
30–32. F. 4. 1959. Chaboissaea decumbens (Swallen) Reeder &
C. Reeder, Phytologia 65(2): 156. 1988.
Muhlenbergia diandra (R. W. Pohl) P. M. Peterson, comb.
nov. Basionym: Pereilema diandrum R. W. Pohl, Novon 2(2):
102. 1992.
Muhlenbergia geminiflora (Kunth) P. M. Peterson, comb.
nov. Basionym: Aegopogon geminiflorus Kunth, Nov. Gen. Sp.
(quarto ed.) 1: 133, t. 43. 1816. Heterotypic synonyms: Lamarkia
tenella DC., Cat. Pl. Hort. Monsp. 120. 1813. Aegopogon tenellus
(DC.) Trin., Gram. Unifl. Sesquifl. 164. 1824. non Muhlenbergia
tenella (Kunth) Trin.
Muhlenbergia ligulata (E. Fourn.) Scribn. & Merr., Bull. Div.
Agrostol. USDA 24. 19. 1901. Basionym: Chaboissaea ligulata
E. Fourn., Mexic. Pl. 2: 112t. 1. 1886.
Muhlenbergia paniculata (Nutt.) P. M. Peterson, comb. nov.
Basionym: Lepturus paniculatus Nutt., Gen. N. Amer. Pl. 1: 81.
1818. Schedonnardus paniculatus (Nutt.) Trel., Annual Rep.
Geol. Surv. Arkansas 1888(4): 236. 1891.
Muhlenbergia pereilema P. M. Peterson, Caldasia 31(2):
293. 2009. Replaced name: Pereilema crinitum J. Presl, Reliq.
Haenk. 1(4–5): 233, t. 37, f. a–f. 1830. non Muhlenbergia
crinita (L. f.) Trin.
Muhlenbergia phalaroides (Kunth) P. M. Peterson, Caldasia
31(2): 294. 2009. Basionym: Lycurus phalaroides Kunth, Nov.
Gen. Sp. (quarto ed.) 1: 142. 1816.
1544
American Journal of Botany
[Vol. 97
Fig. 3. Phylogram of best maximum likelihood tree from analysis of combined plastid and ITS data. Numbers above branches represent bootstrap
values; numbers below branches are posterior probability values. (A) Detail of upper portion and (B) lower portion of phylogram. Abbreviations for subtribes: A = Aeluropodinae, B = Boutelouinae, E = Eleusininae, H = Hilariinae, Mo = Monanthochloinae, Sc = Scleropogoninae, Td = Triodiinae, Tg =
Traginae, Tt = Tridentinae. Taxon color indicates native distribution: green = North America, blue = South America, purple = North and South America,
red = southeast Asia.
September 2010]
Peterson et al.—Phylogeny of Muhlenberginiinae
1545
American Journal of Botany
1546
Muhlenbergia phleoides (Kunth) P. M. Peterson, comb. nov.
Basionym: Lycurus phleoides Kunth, Nov. Gen. Sp. (quarto
ed.) 1: 142, t. 45. 1816.
Muhlenbergia plumosa P. M. Peterson, nom. nov. Replaced
name: Pereilema ciliatum E. Fourn, Mexic. Pl. 2: 93. 1886 non
Muhlenbergia ciliata (Kunth) Trin. Notes: The new name emphasizes the small feathery hairs on the surface of the fascicled spikelets and the sterile bristles that surround the fertile spikelets.
Muhlenbergia subg. Pseudosporobolus (Parodi) P. M. Peterson, comb. stat. nov. Basionym: Muhlenbergia unranked Pseudosporobolus Parodi, Physis. Revista de la Sociedad
Argentina de Ciencias Naturales 9: 207. 1928. M. sect. Pseudosporobolus (Parodi) Pilg., Die Natülichen Planzenfamilien,
Zweite Auflage 14d: 71. 1956. Lectotype: Muhlenbergia fastigiata (J. Presl) Henrard, designated here. Parodi (1928) and Pilger
(1956) did not explicitly indicate the type species for this taxon.
Muhlenbergia shepherdii (Vasey) Swallen, Contr. U. S. Natl.
Herb. 29(4): 204. 1947. Basionym: Sporobolus shepherdii Vasey,
Bull. Torrey Bot. Club 14: 8. 1887. Blepharoneuron shepherdii
(Vasey) P. M. Peterson & Annable, Syst. Bot. 15: 519. 1990.
Muhlenbergia solisii (G. A. Levin) P. M. Peterson, comb.
nov. Basionym: Aegopogon solisii G. A. Levin, Mem. San
Diego Soc. Nat. Hist. 16: 61. 1989.
Muhlenbergia subbiflora Hitchc., N. Amer. Fl. 17(6): 437.
1935. Chaboissaea subbiflora (Hitchc.) Reeder & C. Reeder,
Phytologia 65(2): 156. 1988.
Muhlenbergia tricholepis (Torr.) P. M. Peterson, comb.nov.
Basionym: Vilfa tricholepis Torr., Pacif. Railr. Rep. 4(5): 155.
1857. Blepharoneuron tricholepis (Torr.) Nash, Bull. Torrey
Bot. Club 25(2): 88. 1898.
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Texas, USA.
Taxon
Voucher
Country
ndhF
rpl32-trnL
rps16-trnK
rps3
ITS
rps16 intron
ndhA intron
GU359613
GU360011
GU360578
GU360143
GU359259
GU360274
GU359403
Peterson 22044 & Saarela
Weinert s.n. & Mosawi
Mexico
Iraq
GU359592
GU359591
GU360012
GU360013
GU360577
GU360576
GU360128
GU360085
GU359260
GU359261
GU360278
GU360284
GU359392
GU359391
Hitchcock 7541
Mexico
GU359577
GU360015
GU360573
GU360088
GU359264
GU360318
GU359388
Chalmers 5
Australia
GU359585
GU359861
GU360567
GU360095
GU359286
GU360311
GU359421
Anson s.n.
Australia
GU359584
GU359860
GU360566
GU360113
GU359272
GU360310
GU359420
Peterson 7946, Annable &
Herrera
Melix 570 & Cherobini
Mexico
—
GU359859
GU360550
GU360098
GU359258
GU360309
—
GU359582
GU359857
GU360579
GU360100
GU359275
—
—
Peterson 20013& Sanchez
Alvarado
Peterson 22452 & Saarela
Mexico
—
HM143139
HM143625
HM143242
HM143038
HM143529
HM143346
Mexico
GU359580
GU359854
GU360560
GU360102
GU359277
GU360320
GU359419
Peterson 22099 & Saarela
Mexico
GU359576
GU359853
GU360559
GU360103
GU359278
GU360305
GU359418
Peterson 21994 & Saarela
Mexico
GU359570
GU359852
GU360558
GU360104
GU359279
GU360304
GU359417
Peterson 21423, Saarela &
Stančik
Chaboissaea atacamensis
Peterson 19626, Soreng,
(Parodi) P. M. Peterson & Annable
Salariato, & Panizza,
Chaboissaea ligulata E. Fourn.
Peterson 22416 & Saarela
Chaboissaea subbiflora (Hitchc.) Reeder Peterson 21158, Saarela,
& C. Reeder
Rosen & Reid
Chloris radiata (L.) Sw.
Peterson 22278 & Saarela
Crypsis aculeata (L.) Aiton
Soreng 5469 & Peterson
Cynodon hirsutus Stent
Smook 6616
Dasyochloa pulchella (Kunth)
Peterson 21992 & Saarela
Willd. ex Rydb.
Distichlis spicata (L.) Greene
Peterson 19309, Soreng,
Salariato & Panizza
Eleusine indica (L.) Gaetrn.
Peterson 21362, Saarela
& Flores Villegas
Erioneuron avenaceum (Kunth) Tateoka Peterson 19329, Soreng,
Salariato & Panizza
Gouinia paraguayensis (Kuntze) Parodi Peterson 11526 & Annable
Gymnopogon grandiflorus
Peterson 16642 &
Roseng., B. R. Arill. & Izag.
Refulio-Rodriguez
Hilaria cenchroides Kunth
Peterson 22339 & Saarela
Jouvea pilosa (J. Presl) Scribn.
Peterson 11017 & Annable
Lepturus repens R. Br.
Whistler 9853
Mexico
GU359567
GU359848
GU360606
GU360133
GU359232
GU360296
GU359383
Argentina
GU359729
GU359879
GU360595
GU360115
GU359344
GU360489
GU359382
Mexico
Mexico
GU359718
GU359707
GU359863
GU359877
GU360551
GU360518
GU360069
GU360036
GU359273
GU359318
GU360440
GU360439
GU359381
GU359428
Mexico
China
South Africa
Mexico
GU359724
GU359573
GU359751
GU359689
GU359872
GU359841
GU359876
GU359864
GU360513
GU360599
GU360594
GU360505
GU360048
GU360140
GU360135
GU360039
GU359321
GU359238
GU359229
GU359330
GU360434
GU360402
GU360452
GU360482
GU359366
GU359362
GU359358
GU359369
Argentina
GU359695
GU359801
GU360499
GU360032
GU359346
GU360475
GU359478
Mexico
GU359698
GU359797
GU360496
GU360031
GU359338
GU360472
GU359473
Argentina
GU359773
GU359822
GU360525
GU360063
GU359310
GU360403
GU359441
Argentina
Peru
GU359732
GU359733
GU359817
GU359816
GU360504
GU360581
GU360058
GU360057
GU359314
GU359200
GU360384
GU360383
GU359437
GU359436
Mexico
Mexico
Diego Garcia
Island
Mexico
GU359736
GU359737
GU359730
GU359813
GU359812
GU359893
GU360697
GU360696
GU360691
GU360055
GU360173
GU360228
GU359143
GU359144
GU359150
GU360380
GU360379
GU360428
GU359424
GU359433
GU359427
GU359744
GU359976
GU360688
GU360224
GU359152
GU360426
GU359425
Mexico
GU359745
South Africa GU359746
GU359975
GU359972
GU360687
GU360670
GU360223
GU360206
GU359153
GU359155
GU360425
GU360424
GU359451
GU359453
Blepharidachne benthamiana
(Hack.) Hitchc.
Blepharoneuron shepherdii
(Vasey) P. M. Peterson & Annable
Blepharoneuron shepherdii
(Vasey) P. M. Peterson & Annable
Blepharoneuron tricholepis
(Torr.) Nash
Bouteloua aristidoides
(Kunth) Griseb.
Bouteloua uniflora Vasey
Lycurus setosus (Nutt.)
C. Reeder
Lycurus setosus (Nutt.) C. Reeder
Microchloa caffra Nees
Peterson 20960, Saarela, Lara
Contreras & Reyna Alvarez
Peterson 22008
Smook 10441
Argentina
1549
Mexico
Peterson et al.—Phylogeny of Muhlenberginiinae
Peterson 22045 & Saarela
Aegopogon cenchroides Humb.
& Bonpl. ex Willd.
Aegopogon tenellus (DC.) Trin.
Aeluropus lagopoides (L.)
Trin. ex Thwaites
Allolepis texana (Vasey) Soderstr.
& H. F. Decker
Astrebla pectinata (Lindl.) F. Muell.
ex Benth.
Austrochloris dichanthioides
(Everist) Lazarides
Bealia mexicana Scribn.
September 2010]
Appendix 1. Specimens sampled, vouchers (all housed at the United States National Herbarium, US), country, and GenBank accessions for DNA sequences. Sequences generated by this study
are in boldfaced type; all other sequences are from Peterson et al. (2010).
Monanthochloe littoralis Engelm.
Monelytrum luederitzianum Hack.
Mosdenia phleoides (Hack.) Stent
Muhlenbergia alamosae Vasey
Muhlenbergia andina (Nutt.) Hitchc.
Muhlenbergia angustata
(J. Presl) Kunth
Muhlenbergia angustata
(J. Presl) Kunth
Muhlenbergia annua (Vasey) Swallen
Muhlenbergia appressa C. O. Goodd.
Muhlenbergia arenacea (Buckley)
Hitchc.
Muhlenbergia arenicola Buckley
Muhlenbergia curtifolia Scribn.
Muhlenbergia cuspidata (Torr.
ex Hook.) Rydb.
Muhlenbergia depauperata Scribn.
Muhlenbergia distichophylla
(J. Presl) Kunth
Muhlenbergia dubia E. Fourn.
Muhlenbergia dubia E. Fourn.
Muhlenbergia dumosa Scribn.
ex Vasey
Muhlenbergia durangensis
Y. Herrera
Peterson 19947 &
Lara-Contreras
Peterson 22095 & Saarela
Peterson 22173 & Saarela
Peterson 15208 & Cayouette
Peterson 13386 & Knowles
Peterson 15452, Soreng,
Finot & Judziewicz
Peterson 4760 & Annable
Peterson 22023 & Saarela
McVaugh 22930
Peterson 5013 & Barron
Peterson 14236, Weakley
& LeBlond
Peterson 21965, Soreng
& Montoya Quino
Peterson 22193 & Saarela
Peterson 10768, Annable
& Valdes Reyna
Peterson 5631 & Annable
Hill 35331
Peterson 21293, Saarela
& Flores Villegas
Peterson 15913 &
Valdes Reyna
Peterson 15885 &
Valdes Reyna
Peterson 21105 & Saarela
Peterson 13438, Knowles,
Dietrich & Braxton
Peterson 13644, Knowles,
Dietrich, Braxton &
Gonzalez Elizondo
Peterson 22164 & Saarela
Peterson 22188 & Saarela
Peterson 22096 & Saarela
ndhF
rpl32-trnL
rps16-trnK
rps3
ITS
rps16 intron
ndhA intron
Mexico
South Africa
South Africa
Mexico
USA
GU359748
GU359749
GU359750
HM143436
HM143437
GU359970
GU359969
GU359967
HM143140
HM143141
GU360699
GU360682
GU360681
HM143626
—
GU360235
GU360218
GU360216
HM143243
HM143244
GU359157
GU359158
GU359159
HM143039
HM143040
GU360422
GU360421
GU360420
HM143530
HM143531
GU359460
GU359459
GU359458
HM143347
HM143348
Peru
HM143438
HM143142
HM143627
HM143245
HM143041
HM143532
HM143349
Peru
HM143439
HM143143
HM143628
HM143246
HM143042
HM143533
HM143350
Mexico
USA
Mexico
HM143440
GU359618
GU359619
HM143144
GU359962
GU359961
HM143629
GU360676
GU360675
HM143247
GU360211
GU360210
HM143043
GU359164
GU359165
HM143534
GU360415
GU360414
HM143351
GU359443
GU359452
Mexico
GU359620
GU359960
GU360674
GU360209
GU359166
GU360413
GU359462
Mexico
Mexico
Mexico
Mexico
Chile
HM143441
HM143442
HM143443
—
HM143444
HM143145
HM143146
HM143147
HM143148
HM143149
HM143630
HM143631
HM143632
HM143633
HM143634
HM143248
HM143249
HM143250
HM143251
HM143252
HM143044
HM143045
HM143046
HM143047
HM143048
HM143535
HM143536
HM143537
HM143538
HM143539
HM143352
HM143353
HM143354
HM143355
HM143356
Mexico
Mexico
Mexico
GU359621
HM143445
—
GU359959
HM143150
—
GU360711
HM143635
HM143636
GU360208
HM143253
—
GU359167
HM143049
—
GU360412
HM143540
—
GU359450
HM143357
—
USA
USA
HM143446
HM143447
HM143151
HM143152
HM143637
HM143638
HM143254
HM143255
HM143050
HM143051
HM143541
HM143542
HM143358
HM143359
Peru
HM143448
HM143153
HM143639
HM143256
HM143052
HM143543
HM143360
Mexico
Mexico
HM143449
—
HM143154
—
HM143640
—
HM143257
HM143258
HM143053
—
HM143544
—
HM143361
—
USA
USA
HM143450
—
HM143155
HM143156
HM143641
—
HM143259
HM143260
HM143054
HM143055
HM143545
HM143546
HM143362
—
Mexico
HM143451
HM143157
HM143642
HM143261
HM143056
HM143547
HM143363
Mexico
HM143452
HM143158
HM143643
HM143262
—
HM143548
HM143364
Mexico
HM143454
HM143159
HM143645
HM143264
HM143058
HM143549
HM143366
Mexico
Mexico
HM143453
HM143455
HM143160
HM143161
HM143644
HM143646
HM143263
HM143265
HM143057
HM143059
HM143550
HM143551
HM143365
HM143367
Mexico
HM143456
HM143162
HM143647
HM143266
HM143060
HM143552
HM143368
Mexico
HM143457
HM143163
HM143648
HM143267
HM143061
HM143553
HM143369
Mexico
Mexico
HM143458
GU359622
HM143164
GU359958
HM143649
GU360672
HM143268
GU360207
HM143062
GU359168
HM143554
GU360411
HM143370
GU359449
[Vol. 97
Muhlenbergia elongata Scribn.
ex Beal
Muhlenbergia eludens C. Reeder
Muhlenbergia emersleyi Vasey
Moran 10570
Smook 10031
Schweickerdt 1542
Peterson 22104 & Saarela
Peterson 10432, Annable &
Weinpahl
Peterson 21703, Soreng,
LaTorre & Rojas Fox
Peterson 21958, Soreng &
Montoya Quino
Peterson 22022& Saarela
Peterson 4183 & Annable
Peterson 10624 & Annable
Country
American Journal of Botany
Muhlenbergia argentea Vasey
Muhlenbergia arizonica Scribn.
Muhlenbergia arsenei Hitchc.
Muhlenbergia articulata Scribn.
Muhlenbergia asperifolia (Nees &
Meyen ex Trin.) Parodi
Muhlenbergia brandegeei C. Reeder
Muhlenbergia brevis C. O. Goodd.
Muhlenbergia breviseta Griseb.
ex E. Fourn.
Muhlenbergia californica Vasey
Muhlenbergia capillaris
(Lam.) Trin.
Muhlenbergia caxamarcensis
Lægaard & Sánchez Vega
Muhlenbergia ciliata (Kunth) Trin.
Muhlenbergia crispiseta Hitchc.
Voucher
1550
Appendix 1. Continued
Taxon
Muhlenbergia expansa (Poir.) Trin.
Muhlenbergia fastigiata (J. Presl)
Henrard
Muhlenbergia filiculmis Vasey
Muhlenbergia filiformis
(Thurb. ex S. Watson) Rydb.
Muhlenbergia flavida Vasey
Muhlenbergia flaviseta Scribn.
Muhlenbergia flexuosa Hitchc.
Muhlenbergia glomerata
(Willd.) Trin.
Muhlenbergia grandis Vasey
Muhlenbergia gypsophila
Reeder & C. Reeder
Muhlenbergia himalayensis
Hack. ex Hook. f.
Muhlenbergia huegelii Trin.
Muhlenbergia implicata
(Kunth) Trin.
Muhlenbergia iridifolia Soderstr.
Muhlenbergia jaime-hintonii P. M.
Peterson & Valdés-Reyna
Muhlenbergia jaliscana Swallen
Muhlenbergia japonica Steud.
Muhlenbergia japonica Steud.
Muhlenbergia jonesii (Vasey) Hitchc.
Muhlenbergia lindheimeri Hitchc.
Muhlenbergia longiglumis Vasey
rpl32-trnL
rps16-trnK
rps3
ITS
rps16 intron
ndhA intron
USA
Country
HM143459
HM143165
HM143650
HM143269
HM143063
HM143555
HM143371
Peru
HM143460
HM143166
HM143651
HM143270
HM143064
HM143556
HM143372
Peterson 11954 & Annable
Peterson 10433, Annable &
Weinpahl
Peterson 22237 & Saarela
Peterson 22409 & Saarela
Peterson 20373, Soreng &
Romaschenko
Peterson 22194 & Saarela
Peterson 22260 & Saarela
USA
USA
HM143461
—
HM143167
HM143168
HM143652
HM143653
HM143271
HM143272
HM143065
HM143066
HM143557
HM143558
HM143373
HM143374
Mexico
Mexico
Peru
HM143462
GU359623
HM143463
HM143169
GU359957
HM143170
HM143654
GU360685
HM143655
HM143273
GU360250
HM143274
HM143067
GU359127
HM143068
HM143559
GU360410
HM143560
HM143375
GU359448
HM143376
Mexico
Mexico
HM143464
GU359663
HM143171
GU359966
HM143656
GU360680
HM143275
GU360215
HM143069
GU359160
HM143561
GU360419
HM143377
GU359457
Peterson 22346 & Saarela
Mexico
HM143465
HM143172
HM143657
HM143276
HM143070
HM143562
HM143378
Peterson 21023, Saarela, Lara
Contreras & Reyna Alvarez
Peterson 21180, Saarela,
Gonzalez Elizondo,
Rosen & Reid
Peterson 20924, Saarela
& Howard
Peterson 13413, Knowles,
Dietrich & Braxton
Peterson 15840 &
Valdes Reyna
Soreng 5666, Peterson &
Sun Hang
Soreng 5344, Peterson &
Sun Hang
Peterson 22266, Saarela
Mexico
HM143467
HM143173
HM143658
HM143278
HM143072
HM143563
HM143379
Mexico
HM143466
HM143174
HM143659
HM143277
HM143071
HM143564
HM143380
USA
GU359638
GU359954
GU360716
GU360253
GU359114
GU360407
GU359445
Mexico
HM143468
HM143175
HM143660
HM143279
HM143073
HM143565
HM143381
Mexico
HM143469
HM143176
HM143661
HM143280
HM143074
—
HM143382
China
HM143470
HM143177
HM143281
HM143075
HM143566
HM143383
China
HM143471
HM143178
HM143661
HM143662
HM143663
HM143282
HM143076
HM143567
HM143384
Mexico
HM143472
HM143179
HM143664
HM143283
HM143077
HM143568
HM143385
Peterson 6133 & Annable
Peterson 15841&
Valdes Reyna
Peterson 6149 & Annable
Soreng 5240, Peterson
& Sun Hang
Soreng 5301, Peterson
& Sun Hang
Peterson 4861 & Annable
Peterson 6280 & Annable
Peterson 13666, Knowles,
Dietrich, Braxton &
Gonzalez Elizondo
Peterson 15224 & Cayouette
Peterson 22047 & Saarela
Peterson 22134 & Saarela
Peterson 22062 & Saarela
Mexico
Mexico
HM143473
HM143474
HM143180
HM143181
—
HM143665
HM143284
HM143285
HM143078
HM143079
—
HM143569
—
HM143386
Mexico
China
HM143475
HM143477
HM143182
HM143183
HM143666
HM143667
HM143286
HM143287
HM143080
HM143081
HM143570
HM143571
HM143387
HM143388
China
HM143476
HM143184
HM143668
HM143288
HM143082
HM143572
HM143389
USA
USA
Mexico
HM143478
HM143479
—
HM143185
HM143186
—
HM143669
HM143670
HM143671
HM143289
HM143290
HM143291
HM143083
HM143084
—
—
HM143573
—
HM143390
HM143391
—
USA
Mexico
Mexico
Mexico
HM143480
HM143482
HM143481
GU359624
HM143187
HM143189
HM143188
GU359956
HM143672
HM143673
HM143674
GU360683
HM143292
HM143293
HM143294
GU360265
HM143085
HM143087
HM143086
GU359125
HM143574
HM143576
HM143575
GU360409
−
HM143393
HM143392
GU359447
Peterson 4519 & Annable
Mexico
HM143483
HM143190
HM143675
HM143295
HM143088
HM143577
HM143394
Peterson 21884, Soreng
& Sanchez Vega
Peru
HM143484
HM143191
HM143676
HM143296
HM143089
HM143578
—
1551
Muhlenbergia longiligula Hitchc.
Muhlenbergia lucida Swallen
Muhlenbergia lucida Swallen
Muhlenbergia macroura
(Kunth) Hitchc.
Muhlenbergia majalcensis
P. M. Peterson
Muhlenbergia maxima
Lægaard & Sánchez Vega
Voucher
Peterson et al.—Phylogeny of Muhlenberginiinae
Muhlenbergia fragilis Swallen
Muhlenbergia gigantea (E. Fourn.)
Hitchc.
Muhlenbergia gigantea (E. Fourn.)
Hitchc.
Muhlenbergia glauca
(Nees) B. D. Jacks.
Muhlenbergia glauca
(Nees) B. D. Jacks.
ndhF
Peterson 14234, Weakley
& LeBlond
Peterson 21512, Soreng,
LaTorre & Rojas Fox
September 2010]
Appendix 1. Continued
Taxon
Voucher
Country
ndhF
rpl32-trnL
rps16-trnK
rps3
ITS
rps16 intron
ndhA intron
USA
HM143485
HM143192
HM143678
HM143298
HM143091
HM143579
HM143395
Peterson 5562 & Annable
Peterson 21855 & Soreng
USA
Peru
HM143486
HM143487
HM143193
HM143194
HM143677
HM143679
HM143297
HM143299
HM143090
HM143092
HM143580
HM143581
HM143396
HM143397
Muhlenbergia minutissima (Steud.)
Swallen
Muhlenbergia montana (Nutt.) Hitchc.
Muhlenbergia montana (Nutt.) Hitchc.
Muhlenbergia mucronata (Kunth) Trin.
Muhlenbergia nigra Hitchc.
Muhlenbergia palmeri Vasey
Muhlenbergia palmirensis Grignon &
Lægaard
Muhlenbergia pauciflora Buckley
Muhlenbergia pectinata C. O. Goodd.
Muhlenbergia peruviana (P. Beauv.)
Steud.
Muhlenbergia polycaulis Scribn.
Muhlenbergia porteri
Scribn. ex Beal
Muhlenbergia pubescens
(Kunth) Hitchc.
Muhlenbergia pubescens
(Kunth) Hitchc.
Muhlenbergia pubigluma Swallen
Peterson 22012 & Saarela
Mexico
—
HM143195
HM143680
HM143300
HM143093
—
—
Peterson 22046 & Saarela
Peterson 22234 & Saarela
Peterson 22038 & Saarela
Peterson 16097 & Rosales
Peterson 5478 & Annable
Peterson 9317 & Judziewicz
Mexico
Mexico
Mexico
Mexico
USA
Ecuador
HM143488
GU359705
HM143489
HM143490
HM143491
—
HM143196
GU359964
HM143197
HM143198
HM143199
HM143200
HM143681
GU360678
HM143682
HM143683
HM143684
HM143685
HM143301
GU360213
HM143302
HM143303
HM143304
HM143305
HM143094
GU359162
HM143095
HM143096
HM143097
HM143098
HM143582
GU360417
HM143583
HM143584
HM143585
HM143586
HM143398
GU359455
HM143399
HM143400
HM143401
HM143402
Peterson 22048 & Saarela
Peterson 22108 & Saarela
Peterson 22440 & Saarela
Mexico
Mexico
Mexico
HM143492
HM143493
GU359625
HM143201
HM143202
GU359955
HM143686
HM143687
GU360713
—
HM143306
GU360221
HM143099
HM143100
GU359154
HM143587
HM143588
GU360408
HM143403
HM143404
GU359446
Peterson 22092 & Saarela
Peterson 19846 & Lara
Contreras
Peterson 21250 & Saarela
Mexico
Mexico
HM143494
HM143495
HM143203
HM143204
HM143688
HM143689
HM143307
HM143308
HM143101
HM143102
HM143589
HM143590
—
HM143405
Mexico
HM143496
HM143205
HM143691
HM143310
HM143103
HM143592
HM143406
Peterson 22101 & Saarela
Mexico
HM143497
HM143206
HM143690
HM143309
HM143104
HM143591
HM143407
Peterson 15838 &
Valdes Reyna
Peterson 6227 & Annable
Peterson 16103 & Rosales
Mexico
HM143498
HM143207
HM143692
HM143311
HM143105
HM143593
HM143408
Mexico
Mexico
HM143499
HM143500
HM143208
HM143209
HM143693
HM143694
HM143312
HM143313
HM143106
HM143107
HM143594
—
HM143409
HM143410
Soreng 5302, Peterson & Sun
Hang
Peterson 22447 & Saarela
China
HM143501
HM143210
HM143695
HM143314
HM143108
HM143595
HM143411
Mexico
GU359627
GU359953
GU360717
GU360254
GU359115
GU360406
GU359444
Peterson 21262 & Saarela
Peterson 7900 & Annable
Mexico
USA
HM143502
HM143503
HM143211
HM143212
HM143696
HM143697
HM143315
HM143316
HM143109
HM143110
—
HM143596
HM143412
HM143413
Peterson 6285 & Annable
USA
HM143504
HM143213
HM143698
HM143317
HM143111
HM143597
HM143414
Peterson 19817, Saarela
& Sears
Peterson 7832 & Annable
USA
GU359617
GU359978
GU360677
GU360212
GU359163
GU360431
GU359454
USA
HM143505
HM143214
HM143699
HM143318
HM143112
HM143598
HM143415
Peterson 22129 & Saarela
Peterson 21637, Soreng,
LaTorre & Rojas Fox
Peterson 22061 & Saarela
Peterson 15928 &
Valdes Reyna
Peterson 19443, Soreng,
Salariato & Panizza
Peterson 14843, Blackburn &
Peterson
Mexico
Peru
GU359629
GU359616
GU359951
GU359952
GU360729
GU360718
GU360256
GU360255
GU359117
GU359116
GU360357
GU360405
GU359481
GU359380
Mexico
Mexico
HM143506
HM143507
HM143215
HM143216
HM143700
HM143701
HM143319
HM143320
HM143113
HM143114
HM143599
HM143600
HM143416
—
Argentina
GU359765
GU359950
GU360679
GU360214
GU359161
GU360404
GU359456
USA
HM143508
HM143217
HM143702
HM143321
HM143115
HM143601
HM143417
Muhlenbergia purpusii Mez
Muhlenbergia quadridentata
(Kunth) Trin.
Muhlenbergia ramosa (Hack. ex
Matsum.) Makino
Muhlenbergia ramulosa (Kunth)
Swallen
Muhlenbergia reederorum Soderstr.
Muhlenbergia repens (J. Presl)
Hitchc.
Muhlenbergia reverchonii
Vasey & Scribn.
Muhlenbergia richardsonis
(Trin.) Rydb.
Muhlenbergia richardsonis
(Trin.) Rydb.
Muhlenbergia rigens (Benth.) Hitchc.
Muhlenbergia rigida (Kunth) Kunth
Muhlenbergia rigida (Kunth) Kunth
Muhlenbergia robusta
(E. Fourn.) Hitchc.
Muhlenbergia schreberi J. F. Gmel.
Muhlenbergia sericea (Michx.)
P. M. Peterson
[Vol. 97
Peterson 20861 & Saarela
American Journal of Botany
Muhlenbergia mexicana var.
filiformis (Torr.) Scribn.
Muhlenbergia mexicana (L.) Trin.
Muhlenbergia microsperma (DC.)
Kunth
1552
Appendix 1. Continued
Taxon
Muhlenbergia setifolia Vasey
Muhlenbergia sinuosa Swallen
Muhlenbergia sobolifera (Muhl.
ex Willd.) Trin.
Muhlenbergia speciosa Vasey
Muhlenbergia uniflora
(Muhl.) Fernald
Muhlenbergia utilis (Torr.) Hitchc.
Muhlenbergia vaginata Swallen
Muhlenbergia versicolor Swallen
Muhlenbergia villiflora var. villosa
(Swallen) Morden
Muhlenbergia virescens (Kunth) Trin.
Muhlenbergia virescens (Kunth) Trin.
Muhlenbergia virletii (E. Fourn.)
Soderstr.
Muhlenbergia wrightii Vasey
ex J. M. Coult.
Muhlenbergia x involuta Swallen
Munroa argentina Griseb.
Orinus kokonorica (K. S. Hao)
Keng ex X. L. Yang
Pereilema beyrichianum
(Kunth) Hitchc.
Pereilema ciliatum E. Fourn.
Pereilema crinitum J. Presl
Perotis hordeiformis Nees
Voucher
Country
rps16-trnK
rps3
ITS
rps16 intron
ndhA intron
HM143509
HM143218
HM143703
HM143322
HM143116
HM143602
HM143418
Mexico
—
HM143219
HM143704
HM143323
HM143117
HM143603
HM143419
USA
HM143510
HM143220
—
HM143324
HM143118
HM143604
HM143420
Peterson 13616, Dietrich,
Braxton, & Gonzalez Elizondo
Mexico
HM143511
HM143221
HM143705
HM143325
HM143119
HM143605
HM143421
Peterson 22362 & Saarela
Peterson 15238 & Cayouette
Peterson 13709
Mexico
USA
Mexico
HM143512
HM143513
HM143514
HM143222
HM143223
HM143224
HM143706
HM143707
HM143708
HM143326
HM143327
HM143328
HM143120
HM143121
HM143122
HM143606
HM143607
HM143608
HM143422
—
HM143423
Peterson 21243 & Saarela
Peterson 22053 & Saarela
Mexico
Mexico
HM143515
HM143516
HM143225
HM143226
HM143709
HM143710
HM143329
HM143330
HM143123
HM143124
HM143609
HM143610
HM143424
HM143425
Peterson 22141 & Saarela
Peterson 15778 & Saarela
Mexico
USA
HM143517
HM143518
HM143227
HM143228
HM143711
HM143712
HM143331
HM143332
HM143125
HM143126
HM143611
HM143612
—
HM143426
Peterson 22344 & Saarela
Mexico
HM143519
HM143229
HM143713
HM143333
HM143127
HM143613
HM143427
Peterson 22016 & Saarela
Peterson 5619 & Annable
Mexico
USA
—
HM143520
HM143230
HM143231
HM143714
HM143715
HM143334
HM143335
HM143128
HM143129
HM143614
HM143615
—
HM143428
Peterson 19429, Soreng,
Salariato & Panizza
Peterson 13212, Annable,
Pizzolato, Gordon, Frett,
Frick, Morrone & Griner
Peterson 20862 & Saarela
Argentina
GU359630
GU359992
GU360720
GU360266
GU359118
GU360267
—
USA
HM143521
HM143232
HM143716
HM143337
HM143130
HM143616
HM143429
USA
GU359631
GU359994
GU360715
GU360258
GU359119
GU360275
GU359463
Peterson 5735 & Annable
Peterson 22417 & Saarela
Peterson 9913 & Annable
Peterson 15811 & Valdes
Reyna
Peterson 21259 & Saarela
Peterson 22412 & Saarela
Peterson 9724 & Campos
Villanueva
Peterson 20964, Saarela, Lara
Contreras & Reyna Alvarez
Peterson 6284 & Annable
Peterson 15505, Soreng &
Judziewicz
Soreng 5447, Peterson &
Sun Hang
Peterson 20366, Soreng &
Romaschenko
Peterson 20106, Hall, Alvarez
Marvan & Alvarez Jimenez
Peterson 22191 & Saarela
Soreng 5717, Peterson &
Sun Hang
USA
Mexico
Mexico
Mexico
HM143522
—
—
HM143523
HM143233
HM143234
HM143235
HM143236
HM143717
HM143718
HM143719
HM143720
HM143338
—
HM143339
HM143340
HM143131
—
HM143132
HM143133
HM143617
HM143618
HM143619
HM143620
HM143430
—
—
HM143431
Mexico
Mexico
Mexico
HM143524
HM143525
HM143526
HM143237
HM143238
HM143239
HM143721
HM143722
—
HM143341
HM143342
HM143343
HM143135
HM143134
HM143136
HM143622
HM143621
—
HM143433
HM143432
—
Mexico
HM143527
HM143240
HM143723
HM143344
HM143137
HM143623
HM143434
USA
Chile
HM143528
GU359633
HM143241
GU360006
HM143724
GU360723
HM143345
GU360260
HM143138
GU359121
HM143624
—
HM143435
GU359385
China
GU359628
GU359999
GU360728
GU360259
GU359140
GU360270
GU359399
Peru
GU359597
GU359995
GU360712
GU360247
GU359129
GU360280
GU359493
Mexico
GU359598
GU359979
GU360719
GU360246
GU359130
GU360281
GU359516
Mexico
China
GU359599
GU359600
GU359993
GU359991
GU360710
GU360708
GU360245
GU360243
GU359131
GU359132
GU360282
GU360283
GU359519
GU359520
1553
rpl32-trnL
Mexico
Peterson et al.—Phylogeny of Muhlenberginiinae
Muhlenbergia spiciformis Trin.
Muhlenbergia straminea Hitchc.
Muhlenbergia stricta
(J. Presl) Kunth
Muhlenbergia subaristata Swallen
Muhlenbergia tarahumara
P. M. Peterson & Columbus
Muhlenbergia tenella (Kunth) Trin.
Muhlenbergia tenuiflora
(Willd.) Britton, Sterns & Poggenb.
Muhlenbergia tenuifolia
(Kunth) Kunth
Muhlenbergia texana Buckley
Muhlenbergia thurberi
(Scribn.) Rydb.
Muhlenbergia torreyi (Kunth)
Hitchc. ex Bush
Muhlenbergia uniflora
(Muhl.) Fernald
ndhF
Peterson 20942, Saarela, Lara
Contreras & Reyna Alvarez
Peterson 7976, Annable &
Herrera
Peterson 20834 & Saarela
September 2010]
Appendix 1. Continued
Taxon
Taxon
Redfieldia flexuosa (Thurb.
ex A. Gray) Vasey
Schaffnerella gracilis (Benth.) Nash
Schedonnardus paniculatus
(Nutt.) Trel.
Scleropogon brevifolius Phil.
Sohnsia filifolia (E. Fourn.)
Airy Shaw
Sporobolus cryptandrus
(Torr.) A. Gray
Vaseyochloa multinervosa
(Vasey) Hitchc.
Willkommia sarmentosa Hack.
Zoysia macrantha Desv.
Country
ndhF
rpl32-trnL
rps16-trnK
rps3
ITS
rps16 intron
ndhA intron
Peterson 7845 & Annable
USA
GU359604
GU359985
GU360702
GU360191
GU359138
GU360289
GU359525
Schaffner 134
Peterson 12070 & Annable
Mexico
USA
—
GU359609
GU359981
GU359936
—
GU360673
—
GU360170
—
GU359201
—
GU360375
—
GU359529
Peterson 19280, Soreng,
Salariado & Panizza
Peterson 11129 & Annable
Argentina
GU359611
GU359919
GU360635
GU360167
GU359203
−
GU359530
Mexico
GU359612
GU359918
GU360634
GU360166
GU359204
GU360350
GU359531
Peterson 22003 & Saarela
Mexico
GU359674
GU359914
GU360631
GU360162
GU359208
GU360354
GU359524
Carter 2784
USA
GU359669
GU359920
GU360639
GU360154
GU359217
GU360364
GU359512
FLSP 457
Seydel 448
Peru
GU359675
South Africa GU359601
GU359898
GU359988
GU360616
GU360705
GU360148
GU360240
GU359224
GU359135
GU360370
GU360277
GU359503
GU359522
Peterson 15686 & Soreng
Peterson 21997& Saarela
Peterson 14437, Soreng &
Rosenberg
Swallen 10041
Chile
Mexico
Australia
GU359681
GU359682
GU359683
GU359948
GU359947
GU359946
GU360668
GU360667
GU360666
GU360194
GU360195
GU360205
GU359172
GU359173
GU359174
GU360361
GU360321
GU360322
GU359565
GU359557
GU359550
USA
GU359656
GU359925
GU360646
GU360177
GU359193
GU360342
GU359544
Schweickerdt 2181
Soreng 5913 & Peterson
South Africa GU359657
Australia
GU359660
GU359924
GU360017
GU360645
GU360641
GU360252
GU360020
GU359194
GU359142
GU360343
GU360346
GU359545
GU359558
American Journal of Botany
Swallenia alexandrae (Swallen)
Soderstr. & H. F. Decker
Tragus berteronianus Schult.
Trichoneura eleusinoides
(Rendle) Ekman
Trichoneura weberbaueri Pilg.
Tridens muticus (Torr.) Nash
Triodia basedowii Pritz.
Voucher
1554
Appendix 1. Continued