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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
Phylogenetics, morphological evolution, and classification of
Euphorbia subgenus Euphorbia
Brian L. Dorsey,1,7 Thomas Haevermans,2 Xavier Aubriot,2 Jeffery J. Morawetz,4 Ricarda Riina,5
Victor W. Steinmann6 & Paul E. Berry1,3
1 Department of Ecology and Evolutionary Biology, University of Michigan, 830 North University Avenue, Ann Arbor,
Michigan 48109-1048, U.S.A.
2 Muséum National d’Histoire Naturelle, Département Systématique et Evolution, UMR 7205 CNRS/MNHN Origine,
Structure et Evolution de la Biodiversité, CP 39, 57 rue Cuvier, 75231 Paris cedex 05, France
3 University of Michigan Herbarium, Department of Ecology and Evolutionary Biology, 3600 Varsity Drive, Ann Arbor,
Michigan 48108, U.S.A.
4 Rancho Santa Ana Botanic Garden, 1500 N. College Avenue, Claremont, California 91711, U.S.A.
5 Real Jardín Botánico, CSIC, Plaza de Murillo 2, Madrid 28014, Spain
6 Instituto de Ecología, A.C., Centro Regional del Bajío, A.P. 386, 61600 Pátzcuaro, Michoacán, Mexico
7 Current address: The Huntington Botanical Gardens, 1151 Oxford Road, San Marino, California 91108, U.S.A.
Author for correspondence: Brian L. Dorsey, bdorsey@huntington.org
Abstract Euphorbia subg. Euphorbia is the largest and most diverse of four recently recognized subgenera within Euphorbia
and is distributed across the tropics and subtropics. Relationships within this group have been difficult to discern due mainly
to homoplasious morphological characters and inadequate taxon sampling in previous phylogenetic studies. Here we present
a phylogenetic analysis of E. subg. Euphorbia, using one nuclear and two plastid regions, for the most complete sampling of
molecular sequence data to date. We assign 661 species to the subgenus and show that it is comprised of four highly supported
clades, including a single New World clade and multiple independent lineages on Madagascar. Using this phylogenetic framework we discuss patterns of homoplasy in morphological evolution and general patterns of biogeography. Finally, we present
a new sectional classification of E. subg. Euphorbia comprising 21 sections, nine of them newly described here.
Keywords Euphorbia subg. Euphorbia; Euphorbiaceae; growth forms; ITS; Madagascar; matK ; ndhF ; New World; sectional
classification
Supplementary Material The Electronic Supplement (Figs. S1–S3, Appendix S1) and the alignment files are available in the
Supplementary Data section of the online version of this article (http://www.ingentaconnect.com/content/iapt/tax).
Received: 18 June 2012; revision received: 31 Oct. 2012; accepted: 10 Dec. 2012
INTRODUCTION
Euphorbia L. is one of the largest recognized genera of
flowering plants, with about 2000 species. It has a worldwide
distribution but is especially diverse in arid or semi-arid regions
of the tropics and subtropics. The morphological diversity in
this genus includes geophytes, herbs, shrubs, understory and
canopy trees, and an array of succulent and xerophytic forms.
Despite this vast vegetative variation, the entire genus is united
by a distinctive morphological synapomorphy, the cyathium—a
pseudanthial inflorescence that looks superficially like a typical dicot flower (Steinmann & Porter, 2002; Horn & al., 2012).
This structure is intermediate between a flower and an inflorescence in developmental terms (Prenner & Rudall, 2007) and
is comprised of a cup-like involucre that surrounds multiple
male flowers (reduced to single stamens) and a single female
flower (reduced to a single pistil). From this basic structure
various elaborations have evolved, including colorful subtending bracts, cyathial nectary glands with petaloid appendages,
and fusion or addition of cyathial glands. Some of these cyathial
traits represent synapomorphies for particular clades within
the genus. Despite the information provided by the cyathium
and its variations, relationships among species within Euphorbia based on morphological characters have been shown to be
equivocal in many cases (Steinmann & Porter, 2002).
Previous phylogenetic work based on DNA sequence data
suggests that the evolution of characters in Euphorbia, including growth form, photosynthetic systems, and cyathial form
are highly homoplasious, and that the genus has a complex
biogeographic history leading to its nearly worldwide distribution (Steinmann & Porter, 2002; Haevermans & al., 2004;
Bruyns & al., 2006, 2011; Park & Jansen, 2007; Horn & al.,
2012; Yang & al., 2012). These evolutionary and biogeographic
patterns make Euphorbia an ideal system for the study of complex character evolution and adaptation of plants to different environments. Establishing a well-resolved phylogenetic
framework for the major clades of the genus is a prerequisite
to this research.
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
southern Asia. The species of E. sect. Euphorbia from Africa
and Asia are often compared to the cacti of the New World as
a classic example of convergent evolution, and they are the
prime representatives of stem succulents in E. subg. Euphorbia.
Bruyns & al. (2006) proposed a sectional classification for
E. subg. Euphorbia based almost entirely on Old World species,
but their relatively small taxonomic sampling did not allow for
the establishment of a comprehensive phylogenetic hypothesis
and classification. Even with an expanded sampling of mostly
African and Arabian species from E. subg. Euphorbia (Bruyns
& al., 2011), important groups from Madagascar and the New
World were not well represented in a phylogenetic analysis of
E. subg. Euphorbia; a much broader sampling of the putative
members of E. subg. Euphorbia from across the geographic
range of the subgenus is required to gain a global understanding of the evolutionary relationships in this complex group.
To date, the relationships and phylogenetic position of the
New World species in E. subg. Euphorbia have not been suitably resolved (Steinmann & Porter, 2002; Bruyns & al., 2006).
The 26 New World species in E. subg. Euphorbia included by
Zimmerman & al. (2010) formed a grade in their analysis of ITS
and trnL-trnF chloroplast spacer data, but the eleven species
sampled by Horn & al. (2012) for their ten-locus study formed
a well-supported clade. The placement of the New World members of E. subg. Euphorbia and determining whether they represent a single clade is one of the main aims of this study.
Another key question involves an ecologically and morphologically diverse set of approximately 120 species from
Madagascar. In contrast to other well-defined Old World
groups, such as E. sect. Euphorbia and E. sect. Monadenium,
the Madagascan species are the least understood group of
species in E. subg. Euphorbia from a phylogenetic standpoint
(Steinmann & Porter, 2002; Haevermans & al., 2004; Bruyns
& al., 2006; Park & Jansen, 2007; Zimmermann & al., 2010;
Horn & al., 2012). The Madagascan species include, among
others, the crown-of-thorns complex (E. milii and allies) and
coraliform, pencil-stemmed trees such as E. tirucalli and
E. alluaudii. There have been two clades of Madagascan species resolved in all previous phylogenetic studies involving
E. subg. Euphorbia, but their relationship to each other has
not been well resolved. All of the pencil-stemmed species in
Euphorbia have previously been placed in one group, E. sect.
Tirucalli, (e.g., Boissier, 1862; Hassall, 1977), but there is ample
evidence now that this previous circumscription of E. sect.
Tirucalli does not represent a monophyletic group (Boissier,
1862; Hassall, 1977; Steinmann & Porter, 2002; Haevermans,
2003; Haevermans & al., 2004; Bruyns & al., 2006; Barres
& al., 2011; Horn & al., 2012; Yang & al., 2012). Also, there are
Fig. 1. Examples of morphological diversity in E. subg. Euphorbia. A–F, Growth forms: A, herb, E. floridana; B, leafy shrub with long- and shortshoots, E. hedyotoides; C, cactiform succulent, E. cooperi ; D, geophyte, E. nana; E, spiny, xerophytic shrub, E. horombensis; F, pencil-stem
tree, E. decorsei. G–L, Cyathial variations: G, simple dichasial form of E. sect. Euphorbia, E. inarticulata; H, spreading cyathophylls common in
E. sect. Goniostema, E. horombensis; I, zygomorphic cyathium with nectar spur typical of E. sect. Crepidaria, E. calcarata; J, fused glands of
E. sect. Monadenium, E. heteropoda; K, horned glands of E. sect. Brasilienses, E. sipolisii ; L, cyathophylls forming a pseudofloral tube typical
of several members of E. sect. Goniostema, E. viguieri. M–P, Spine structures: M, comb-like stipular spines in E. sect. Goniostema, E. viguieri ;
N, spine-shields in E. sect. Euphorbia, E. zoutpansbergensis; O, stipular spines in E. sect. Goniostema, E. milii ; P, spines of E. neospinescens,
E. sect. Monadenium. — Photo credits: A: K. Gulledge, Atlas of Florida Vascular Plants (http://www.florida.plantatlas.usf.edu/); D: S. Dutta;
I: P. Carillo-Reyes; L, M: B. van Ee; O: F. Vincentz (www.euphorbia.de).
292
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Over the past decade, molecular phylogenetic studies have
made much progress in understanding the broad-scale relationships within Euphorbia (Steinmann & Porter, 2002; Bruyns
& al., 2006, 2011; Park & Jansen, 2007; Horn & al., 2012; Yang
& al., 2012). Steinmann & Porter (2002) circumscribed Euphorbia as the clade including all species with cyathia and furthermore established the presence of four major clades within the genus. Bruyns & al. (2006) formally recognized these four clades
as subgenera: E. subg. Esula Pers., E. subg. Rhizanthium (Boiss.)
Wheeler, E. subg. Chamaesyce Raf., and E. subg. Euphorbia.
Peirson & al. (in prep.) have since determined that E. subg.
Athymalus Neck. ex Reichb. is an earlier valid name for E. subg.
Rhizanthium. Horn & al. (2012) analyzed ten gene regions from
all three plant genomes to firmly establish that E. subg. Esula
is the first clade to diverge, followed by E. subg. Athymalus,
which is sister in turn to the clade of E. subg. Chamaesyce and
E. subg. Euphorbia. With the relatively sparse taxon sampling
in all previous phylogenetic studies, many species in Euphorbia
had not been placed to their corresponding subgenus, and relationships within the subgenera are still incompletely resolved.
From an evolutionary and taxonomic standpoint, there is a need
to develop a comprehensive sectional classification for each of
the subgenera. In this study we attempt to resolve these issues in
E. subg. Euphorbia, which is the largest subgenus in Euphorbia.
Euphorbia subg. Euphorbia contains over 650 species, and
it is the most diverse of the four subgenera in terms of cyathial
variation, growth form, and habitat (Horn & al., 2012). Variation in cyathial morphology in this subgenus is particularly
high and had been the basis for previously recognizing five segregate genera. These segregates include E. sect. Monadenium
(including the former genera Monadenium Pax + Synadenium
Boiss. + Endadenium L.C. Leach) from eastern tropical Africa,
E. sect. Crepidaria (represented by the former genus Pedilanthus Neck.) from Mexico and the Caribbean, and E. sect.
Cubanthus (the former genus Cubanthus (Boiss.) Millspaugh)
from the Caribbean. Each of these groups displays a unique
variation on the basic cyathial form. The genus Elaeophorbia was also previously segregated based on the possession of
fleshy fruits, a rare character state in Euphorbia. Species of
E. subg. Euphorbia include herbs, geophytes, woody shrubs,
understory and canopy trees, stem succulents that range from
dwarf shrubs to candelabriform trees, and the unusual growth
form of pencil-stemmed plants (e.g., E. decorsei, Fig. 1F).
Woody shrubs and trees occur in both xeric and mesic forests
of Madagascar and in the New World tropics. Herbaceous species are found in South America, Africa, and Australia. Geophytes have evolved several times in E. subg. Euphorbia and
are found in Africa, Madagascar, the Arabian Peninsula, and
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
a number of poorly studied leafy species, such as E. pervilleana
from Madagascar, which have been placed in E. sect. Tirucalli
by Bruyns & al. (2006), but are likely part of a separate clade
(Haevermans & Labat, 2004). Because the position of these
species within E. subg. Euphorbia has not been congruent
among previous studies, we still do not know if the Madagascan species form a single clade or represent two or more
independent radiations on the island.
As part of the worldwide Euphorbia Planetary Biodiversity
Inventory (PBI; www.euphorbiaceae.org) project, the goals of the
present study are to: (1) produce a robust phylogenetic hypothesis
of the relationships of all major groups in E. subg. Euphorbia
based on a thorough taxonomic and geographic sampling and
utilizing multiple regions of DNA sequence data, (2) establish the
phylogenetic position of as many members of E. subg. Euphorbia
as possible, and (3) create a sectional classification system for
the subgenus. We plan to use this phylogenetic framework to
address the outstanding phylogenetic questions within E. subg.
Euphorbia, as mentioned above. In particular, we aim to determine if the New World species form a monophyletic group and
to resolve the relationships of the Madagascan species.
MATERIALS AND METHODS
Taxonomic sampling. — A total of 317 accessions representing 226 species of Euphorbia were analyzed in this study,
including ten outgroup species representing the three other
subgenera within the genus. Taxa were selected to obtain a
broad and thorough sampling of putative members of E. subg.
Euphorbia across its geographic range based on previous
molecular phylogenetic studies and the collective knowledge
of the collaborators within the Euphorbia PBI project. Material for DNA extraction was collected by the authors and by
additional PBI collaborators from live plants in the field or in
living collections, as well as from herbarium collections. Live
tissue was preserved in silica gel prior to extraction. Vouchers
of wild specimens were collected as whole or partial plants and
deposited at MICH and/or local herbaria (see Electr. Suppl.:
Appendix S1). Greenhouse specimens were documented with
digital photographs because destructive sampling was discouraged by collection owners. In this case, photo voucher specimens were made using a set of printed photographs from each
sampled specimen and deposited at MICH.
DNA extraction, amplification, and sequencing. — Total
genomic DNA was extracted using the DNeasy Plant Mini Kit
(Qiagen Inc., Valencia, California, U.S.A.) following the manufacturer’s instructions with slight modification for herbarium
material. DNA was diluted 10 to 50 times to reduce inhibition
of PCR enzymes by secondary compounds. Primer pairs were
chosen for this study based on their previous utility in phylogenetic studies of Euphorbia or preliminary tests for polymerase
chain reaction (PCR) amplification specificity, phylogenetic
information content, and absence of long polyA/T regions that
may interrupt sequencing reactions (Steinmann & Porter, 2002;
Haevermans & al., 2004; Bruyns & al., 2006; Steinmann & al.,
2007). The final regions chosen were the cpDNA coding region
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matK including the partial trnK intron, the cpDNA coding
region ndhF, and the internal transcribed spacer region of the
nuclear ribosomal DNA (ITS). All PCR reactions from genomic
DNA were carried out using Ex Taq taq-polymerase and buffer
(Takara Bio Inc., Otsu, Shiga, Japan).
The ndhF gene was PCR-amplified in two pieces: the 5′
half was amplified using primers 536F and 1318R (Olmstead
& Sweere, 1994), and the 3′ half using primers 972F (Olmstead
& Sweere, 1994) and 2110Ri (Steinmann & Porter, 2002). The
15 µl PCR mixture contained 1.5 μL 10× Ex Taq Buffer, 1.2 μL
dNTP (2.5 mM), 0.4–0.6 μL of each primer (10 μM), 0.075 μL
of 5 units/μL Ex Taq, 2–2.5 μL of diluted template DNA and the
remainder of ddH2O. The PCR protocol consisted of an initial
denaturing step of 95°C for 2 min followed by 35 cycles of denaturing at 95°C for 45 s, annealing at 53.8°C for 45 s, extension
at 65°C for 3 min and then a final extension step at 65°C for
5 min (modified from Shaw & al., 2005). The matK region was
amplified using the primers trnK570F and matK1710R (Samuel
& al., 2005). The 15 µl PCR mixture contained 1.5 μL 10× Ex
Taq Buffer, 1.2 μL dNTP (2.5 mM), 0.5 μL of each primer
(10 μM), 0.12 μL of 5 units/μL Ex Taq, 2 μL of diluted template
DNA and the remainder of ddH2O. The PCR protocol consisted
of an initial denaturing step of 95°C for 2 min followed by 35
cycles of denaturing at 95°C for 45 s, annealing at 57°C for 45 s,
extension at 65°C for 5 min and then a final extension step at
65°C for 10 min (modified from Shaw & al., 2005). The ITS
region was amplified using the primers ITS-I (Urbatsch & al.,
2000) and ITS4 (White & al., 1990). The 15 µl PCR mixture
contained 1.5 μL 10× Ex Taq Buffer, 1.2 μL dNTP (2.5 mM),
0.5 µl of 5M Betaine solution (Sigma-Aldrich, Inc., St. Louis,
Missouri, U.S.A.), 0.5 μL of each primer (10 μM), 0.12 μL
of 5 units/μL Ex Taq, 2 μL of diluted template DNA and the
remainder of ddH2O. A touchdown PCR protocol was used for
the ITS region with an initial denaturing step at 95°C for 2 min
and a final extension at 72°C for 15 min. The intervening 35
cycles each had a 2 min denaturing step of 30 s at 95°C and
an extension step of 45 s at 72°C. The annealing temperature
was decreased from 60°C to 50°C as follows: 1 cycle at 60°C,
2 cycles at 59°C, 3 cycles at 58°C, 4 cycles at 57°C, 5 cycles at
55°C, 6 cycles at 52°C, and 14 cycles at 50°C.
All PCR products were examined by gel electrophoresis
on 1% agarose gels. Specific PCR products were purified using
ExoSap-IT (USB Corporation, Cleveland, Ohio, U.S.A.). For
weak PCR products, or products with primer dimers, the QIAquick PCR Purification Kit was used. All PCR products were
sequenced at the University of Michigan DNA Sequencing
Core. ITS and ndhF PCR products were sequenced using the
amplification primers. To maximize bidirectional reads for the
entire length of the matK region, the matK80F primer (Samuel
& al., 2005) and three custom primers (matK688R [5′-CRA
GAT GRA TGG GRT AMG G-3′], matK1850R [CGT CCT
CTA TAT AAC TTG CGC G], matK1387F [CAG TAG GAC
ATC CTA TTA GTA AAC CG]) were used in addition to amplification primers for sequencing.
DNA sequence alignment and models of evolution. —
All ABI chromatograms from sequencing were edited and
assembled using the Staden software package (v.2.0; Staden,
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
1996). All sequences are deposited in GenBank, and species
names, vouchers, and GenBank accession numbers are given
in Appendix S1 (Electr. Suppl.). Sequences of each region
were aligned using the MUSCLE web server at http://www
.ebi.ac.uk/Tools/msa/muscle (Edgar, 2004) and adjusted manually using the program BioEdit v.7.1.3 (Hall, 1999) to maximize
the similarity among sequences in the relatively few regions
in which MUSCLE unnecessarily created multiple gaps when
fewer gaps could be inferred (Simmons, 2004). Some regions
of the partial trnK intron flanking the matK gene were difficult
to unambiguously align and were excluded from the alignment. In total, seven data matrices were assembled. For the
maximum likelihood (ML) analyses all accessions were included to produce matrices for each of the individual regions,
the cpDNA regions concatenated, and all regions concatenated
(matK, ndhF, ITS, cpDNA, and 3-gene matrices, respectively).
A reduced taxon set that minimized missing data was used to
construct concatenated matrices of the cpDNA (cpDNA-min)
and of all regions (3-gene-min) for the Bayesian analyses (see
below). Indels were coded as binary characters for the matK and
the ndhF regions using the simple coding method of Simmons
& Ochoterena (2000) as implemented in the program SeqState
v.1.4.1 (Müller, 2005, 2006). ITS indels were not coded because many were part of ambiguously aligned sections that
were more common and spreadout in the ITS matrix than in
the chloroplast datasets. The best-fitting model of sequence
evolution for each of the three individual matrices was selected
using Modeltest v.3.07 (Posada & Crandall, 1998), employing
the Akaike information criterion (AIC). Modeltest chose the
GTR + I + γ model of nucleotide substitution for all regions and
concatenated datasets except matK, for which the TVR + I + γ
model was chosen. However, because MrBayes does not allow
this model to be specified, and to avoid potential parameter
interactions by modeling among-site rate variation with two
parameters (RAxML manual, v.7.0.4), we used the GTR + γ
model for all analyses.
Phylogenetic inference. — Separate data partitions were
defined for each gene region and character type (DNA or indel), and for codon position within the ndhF region. In the
alignment of the matK region, which includes the trnK intron
and many more gaps across the entire matrix, we were unable
to identify a reliable open reading frame across sequences.
We therefore decided not to treat codon positions as separate
partitions in the analysis. Maximum likelihood estimation
(MLE) of phylogeny and model parameters was performed
using the program RAxML v.7.2.8 (Stamatakis, 2006). Where
applicable, all model parameters except for branch lengths were
estimated separately for each partition. Branch lengths were
estimated as the average across partitions. Matrices were analyzed using the rapid bootstrap (1000 pseudoreplicates) plus
thorough MLE search option [-f a]. Bayesian inference (BI)
of phylogeny and model parameters was performed on the
cpDNA-min and 3-gene-min matrices using MrBayes v.3.2.1
(Huelsenbeck & Ronquist, 2001; Ronquist & Huelsenbeck,
2003). Six independent MCMC runs of four chains each were
run for 14.8 × 107 generations sampling every 104 generations.
Stationarity and convergence of the MCMC runs was assessed
using the programs Tracer v.1.5 (Rambaut & Drummond, 2007)
and online version of AWTY (http://ceb.csit.fsu.edu/awty, Wilgenbusch & al., 2004). Preliminary analyses were used to determine the appropriate parameters for the MCMC runs with
the following results. To achieve swap frequencies of 20% to
60% between adjacent heated chains, the temperature parameter was set to 0.02. To prevent unrealistically long tree length
estimates, the mean of the prior distribution of tree lengths
was adjusted as suggested by Marshall (2010) to a final value
of 250 [brlenspr = unconstrained: exponential (250)]. Reduced
taxa matrices were used because original matrices failed to
converge on a single posterior distribution of tree and model
parameters. Recent studies have found that Bayesian analyses
can be biased by missing data, potentially due to improper
branch length estimation (Marshall & al., 2006; Lemmon & al.,
2009; Marshall, 2010). These matrices contained approximately
30% missing data due to variation in sequencing success for
regions among taxa. In preliminary analyses of both the cpDNA matrix and the 3-gene matrix, each with all taxa included,
multiple independent runs appeared to converge on a particular
log likelihood (LnL) and tree length (TL) distribution while
other runs converged on a markedly different distribution of
each parameter. In these cases a higher mean LnL was consistently associated with a lower mean TL. When the proportion
of missing data in the matrices was reduced to approximately
10% (including gaps) by removing most taxa without all three
regions sequenced, much better performance of the MCMC
chains was achieved in terms of chain swap frequencies, mixing of chains, and convergence of all parameters.
Assessment of clade membership. — Morphological and
geographic distribution data were compiled from herbarium
collections, live collections, field observations, and the literature
for all species included in our molecular datasets as well as any
that were previously classified as closely related to these species
or suspected to belong in E. subg. Euphorbia. These data were
used to determine whether Euphorbia species not sampled for
molecular sequence datasets belong to E. subg. Euphorbia and
to assign these species to clades within the subgenus.
RESULTS
Individual datasets. — Summary statistics for each dataset
are given in Table 1. The matK data provided the greatest information across all levels of the subgenus, while ndhF was less
informative, although it did provide support for major clades.
The ITS data supported some major clades but provided little
resolution regarding relationships among them, and was most
informative for closely related groups (Electr. Suppl.: Fig. S1).
The ML analyses of the individual ndhF and matK datasets
resulted in trees with some topological incongruence but no
instances of well-supported conflict (trees not shown), so these
were concatenated for the cpDNA analyses. We found eight
instances of topological incongruence between the ITS phylogeny and the concatenated cpDNA phylogeny (Electr. Suppl.:
Figs. S1, S2) where both of the alternate topologies had bootstrap support (BS) over 80%. One of these involved the sister
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TAXON 62 (2) • April 2013: 291–315
Table 1. Summary statistics of datasets used for phylogenetic inference. cpDNA dataset
consisted of concatenated matK and ndhF sequences and indel data. 3-gene dataset consisted of concatenated cpDNA and ITS sequences.
matK
cpDNA
3-gene
Number of accessions
177
162
281
232
314
Aligned sequence length
2115
1435
689
3550
4239
Variable DNA sites (%)
810 (39)
545 (38)
456 (66)
–
–
Indels coded
99
38
–
137
137
relationship of two species in E. sect. Monadenium and the
other six the placement of species within E. sect. Euphorbia.
Both of these sections are well-supported clades in all analyses.
Notable among these incongruences, however, is the placement of E. abdelkuri and E. lacei. In the ITS tree, E. abdelkuri
is sister to the rest of E. sect. Euphorbia and E. lacei is the
next to diverge, while in the cpDNA tree these species are
nested within the section close to a group of Indian species
that includes E. antiquorum and E. lactea. Given that the few
instances of conflict were within a single strongly supported
clade, all datasets were concatenated for the 3-gene analysis.
Phylogenetic results. — Figure 2 shows the ML tree from
the 3-gene dataset. This phylogeny is largely congruent with
the cpDNA and ITS trees; the few exceptions are noted below
(Fig. 2; Electr. Suppl.: Figs. S1, S2). The ML tree includes the
most complete taxon sampling of E. subg. Euphorbia, so we
chose to use this tree as the best estimate of the phylogeny.
All datasets recovered a monophyletic E. subg. Euphorbia
consisting of four major lineages (Fig. 2; Electr. Suppl.: Figs.
S1–S3). These clades can be distinguished by their geographic
distributions and we refer to them as the Pacific clade, the
New World clade, Old World clade I, and Old World clade II
(Fig. 2). Support for each of the major lineages is high (BS >
99%, posterior probability [PP] > 0.95) from all datasets, with
the exception of the ITS support for the New World clade and
Old World clade II (BS 28% and 79%, respectively); however,
the relationships among these clades are not well-supported
(Fig. 2; Electr. Suppl.: Figs. S1–S3). One species from Madagascar in our sampling, E. mandravioky, which represents E. sect.
Pachysanthae, a newly defined section in E. subg. Euphorbia,
is not well supported as part of any of the four major clades by
any dataset. It is sister to Old World clade I in the cpDNA (BS
78%) and 3-gene trees (BS < 50%) and sister to Old World clade
II in the ITS tree (BS 54%; Fig. 2; Electr. Suppl.: Figs. S1, S2).
The position of E. mandravioky as sister to Old World clade I
has the highest BS and makes the most sense geographically
given that Old World clade I is mainly a Madagascan clade.
Two additional topological incongruences exist between the
ITS, cpDNA and 3-gene trees. First, E. abdelkuri and E. lacei
are strongly supported as sister to the rest of E. sect. Euphorbia
in the 3-gene tree (BS 93%) or moderately supported as successive sister lineages in the ITS tree (BS 81%). In contrast,
their nested position in the cpDNA tree is well-supported (BS
100%), and the relationships at the base of E. sect. Euphorbia
lack strong support. Second, the position of E. sect. Rubellae,
from northeast Africa, is incongruent between the concatenated
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ITS
ndhF
datasets. In the 3-gene tree, E. sect. Rubellae is sister to the
rest of Old World clade II with BS 68%. In the cpDNA tree this
section is nested within Old World clade II (BS 82%) and sister
to the clade of E. sect. Monadenium and E. sect. Euphorbia (BS
77%). We note that while we chose the 3-gene tree to represent
our best estimate of the phylogeny of E. subg. Euphorbia, the
cpDNA data resolve the relationships within Old World clade
II with higher support. However, because the matK matrix did
not include E. sect. Rubellae, its position in the cpDNA tree is
determined by the ndhF data only.
Among the MrBayes runs that had converged on the same
posterior probability distribution, we discarded those that likely
had not converged on the same distribution of trees, based on
their substantially different support for individual clades (determined with the AWTY Compare analysis). However, for each
dataset there were two runs from which the AWTY Compare
plots of posterior probabilities for clades were very close to
the unity line, indicating that they had converged on the same
distribution of trees. These runs were used to determine support for clades. The Cumulative analyses in AWTY for both
the cpDNA-min and 3-gene-min datasets indicated that runs
that had likely converged reached stationarity by generation
1.2 × 107. All prior trees were discarded as burn-in. Although
the difference in taxon sampling among inference methods
does not allow for detailed comparisons between the Bayesian
and ML trees, the topology of the 50% majority-rule consensus
tree from the Bayesian analysis was generally congruent with
the ML tree (e.g., the same major clades were recovered). The
posterior probabilities of major clades and sections in E. subg.
Euphorbia are summarized in Fig. S3 (Electr. Suppl.).
Taxonomic results. — The phylogenetic hypothesis presented here along with a review of morphological and geographic distribution data allowed us to assign 661 species to
E. subg. Euphorbia and place all of these species to sections.
These sections are indicated on Fig. 2 and are detailed below
in the taxonomic treatment, where we newly define or significantly recircumscribe 11 sections, resulting in a total of
21 sections within E. subg. Euphorbia. The new sections are
concentrated in the New World and Madagascar clades.
DISCUSSION
With our greatly increased sampling effort, we confirmed the results of several previous studies, which found
that Euphorbia subg. Euphorbia is a strongly supported mono-
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
phyletic group (Steinmann & Porter, 2002; Bruyns & al., 2006;
Zimmermann & al., 2010; Horn & al., 2012). Our analyses also
show that the subgenus is comprised of four strongly supported
clades: the New World clade, the Pacific clade (E. sect. Pacificae), Old World clade I, and Old World clade II, although the
relationships among them are not well-supported (Fig. 2). The
lack of resolution along the backbone of the subgenus in this
and all previous studies, and the very short branch lengths at
this level of the tree (data not shown), suggest that the lack of
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Pacific Clade
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E. attastoma
E. phosphorea
sect. Brasilienses
E. sipolisii
E. phosphorea 2
E. attastoma 2
E. heterodoxa
E. lagunillarum
sect. Stachydium
E. comosa
E. comosa 2
E. cymbifera
E. lomelii
E. bracteata
sect. Crepidaria
E. colligata
E. calcarata
E. finkii
E. personata
E. tithymaloides
E. caespitosa
E. portulacoides
E. portulacoides 2
E. portulacoides 4
E. portulacoides 3
E. sp. 1
sect. Nummulariopsis
E. elquiensis
E. elodes
E. peperomioides
E. thinophila
E. papillosa
E. telephioides
E. rosescens
E. germainii
sect. Portulacastrum
E. xylopoda
sect. Calyculatae
E. calyculata
E. pteroneura
E. hoffmanniana
E. dussii
E. weberbaueri
sect. Euphorbiastrum
E. cestrifolia
E. laurifolia
sect. Mesophyllae
E. sinclairiana
E. lactiflua
sect. Lactifluae
E. umbelliformis
E. gymnonota
E. punicea
E. cubensis
sect. Cubanthus
E. podocarpifolia
E. helenae
E. munizii
E. tanquahuete
sect. Tanquahuete
P
E. haeleeleana
P
E. boophthona
P
E. plumerioides
sect. Pacificae
E. stevenii
P
P
E. sarcostemmoides
E. tannensis
E. planiticola
E. aequoris
subg.
E. spinea
E. cotinifolia
Chamaesyce
Habit
E. guiengola
Leafy Tree/Shrub
E. plagiantha
Herb
E. gariepina
subg.
Geophyte
E. bongensis
E. hadramautica
Athymalus
Spiny xerophyte shrubs
E. horrida
Pencil-stem
E. orthoclada
Green-stem succulent
subg.
E. aphylla
E. helioscopia
Esula
E. hirsuta
New World
Clade
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resolution is not an artifact of marker choice but rather a “true”
signal, which may be the result of a rapid radiation early in the
evolutionary history of the subgenus. In addition, by comparing
our results with those of Horn & al. (2012), we do not see an
improvement of the support values in this part of the phylogeny through an increase in taxon sampling. Below we discuss
significant morphological characters within each major clade
and then discuss general patterns of morphological evolution
within the subgenus.
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Distribution
Madagascar
Africa / Arabia
Asia
N. America
C. / S. America
Caribbean
P S. Pacific
Fig. A–C. Maximum-likelihood estimate of the phylogenetic relationships of E. subg. Euphorbia based on the combined matrix of ITS, ndhF,
and matK sequences. For clarity, multiple accessions from species shown to be exclusive lineages are excluded from the tree. Bootstrap support
for clades > 50% is given above branches. Habit (left column) and distribution (right column) are indicated to the left of the taxa names—see
inset for symbol definitions. Sections circumscribed in this study are indicated by shading and are named to the right of the taxa; the four major
clades within E. subg. Euphorbia are indicated to the right of the sectional classification. A, Outgroups and New World clade; B, Pacific clade,
Old World clade I and Old World clade II (in part); C, Old World clade II (in part).
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TAXON 62 (2) • April 2013: 291–315
E. kimberleyana
E. lugardiae
E. schubei
E. guentheri
E. heteropoda
E. rhizophora
E. succulenta
E. neomontana
E. neostolonifera
E. neorubella
E. invenusta
E. pseudolaevis
E. pseudostellata
E. bisellenbeckii
E. neoreflexa
E. lindenii
E. major
E. neovirgata
E. pseudotrinervis
E. sp. 13
E. bicompacta
E. pseudomollis
E. umbellata
E. torrei
E. neospinescens
E. neogossweileri
E. neoarborescens 2
E. magnifica
E. neoarborescens
E. spectabilis
E. neococcinea
E. neogracilis
E. sp. 14
E. sp. 11
E. hedyotoides
E. sp. 9
E. sp. 10
E. sp. 8
E. famatamboay
E. alluaudii
E. cedrorum
E. viguieri
E. aff. retrospina
E. horombensis
E. capuronii
E. sp. 17
E. aff. mahafalensis
E. pedilanthoides
E. didiereoides
E. croizatii
E. lophogona
E. milii
E. capsaintemariensis
E. capsaintemariensis 2
E. rossii
E. tulearensis
E. beharensis
E. ambovombensis
E. decaryi
E. cylindrifolia
E. francoisii
E. geroldii
E. alfredii
E. neohumbertii
E. neohumbertii 2
E. iharanae
E. rubella
E. brunellii
E. arahaka 4
E. kamponii
E. stenoclada
E. tirucalli
E. decorsei
E. enterophora 2
E. arahaka 3
E. arahaka
E. arahaka 2
E. xylophylloides 2
E. xylophylloides
E. enterophora
E. fiherenensis
E. fiherenensis 2
E. stenoclada 2
E. arbuscula
E. damarana
E. dhofarensis
E. gummifera
E. sp. 12
E. sp. 6
E. sp. 5
E. sp. 3
E. sp. 4
E. sp. 2
E. randrianjohanyi
E. tetraptera
E. sp. 7
E. pervilleana
E. rauhii
E. intisy
E. mandravioky
Fig. 2B
sect.
Monadenium
Old World
Clade II
(in part)
sect. Denisophorbia
sect. Deuterocalli
sect. Goniostema
sect. Rubellae
Habit
Leafy Tree/Shrub
Herb
Geophyte
Spiny xerophyte shrubs
Pencil-stem
Green-stem succulent
Distribution
Madagascar
Africa / Arabia
Asia
N. America
C. / S. America
Caribbean
P S. Pacific
sect. Tirucalli
Old World
Clade I
sect. Pervilleanae
sect. Pachysanthae
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
New World clade. — All species from the New World
shown here to belong to E. subg. Euphorbia are included in a
single clade that is highly supported in all but the ITS analysis
(Fig. 2; Electr. Suppl.: Figs. S1–S3). The geographic distribution
of species in E. subg. Euphorbia (Fig. 2) suggests that there has
been a split between New World and Old World clades early in
the history of E. subg. Euphorbia, although confidence in this
interpretation is limited by the low support for the relationships among the Old World clades and the uncertain position
of E. sect. Pachysanthae. New World species have been placed
in E. subg. Euphorbia in previous studies (Steinmann & Porter,
2002; Bruyns & al., 2006; Zimmermann & al., 2010), but our
sampling and sequence data are the first to show the extent
of the New World lineage and to demonstrate its monophyly.
The New World clade consists of 11 highly supported clades
or single species which we treat here as sections. They range
in size from a single species in E. sect. Lactifluae to 36 species in E. sect. Nummulariopsis. The branches that connect
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E. grandicornis 2
E. pseudocactus
E. grandicornis
E. breviarticulata
E. pseudoburuana
E. bougheyi
E. bussei
E. brevitorta
E. bussei 2
E. lividiflora
E. cooperi
E. groenewaldii
E. enormis
E. cactus
E. fractiflexa
E. longispina
E. robecchii
E. ledienii
E. curvirama
E. caerulescens
E. triangularis
E. caerulescens 2
E. keithii
E. perangusta
E. limpopoana
E. avasmontana
E. ammak
E. clivicola
E. lenewtonii
E. ambroseae
E. cuprispina
E. parciramulosa
E. heterospina
E. heterochroma
E. heterospina 2
E. elegantissima
E. heterochroma 2
E. sudanica 3
E. venenifica
E. sudanica
E. sudanica 2
E. unispina
E. sapinii
E. resinifera
E. fruticosa
E. seibanica
E. classenii
E. micracantha
E. stellata
E. persistentifolia
E. griseola
E. decidua
E. fanshawei
E. ingens
E. abyssinica
E. desmondii
E. drupifera 2
E. drupifera
E. nivulia 2
E. neriifolia
E. nivulia
E. nivulia 3
E. neriifolia 2
E. caducifolia
E. teke
E. sp. 16
E. sp. 15
E. antiquorum
E. antiquorum 2
E. lactea
E. vajravelui
E. evansii
E. grandidens
E. ramipressa
E. tanaensis
E. confinalis
E. sekukuniensis
E. tetragona
E. abdelkuri
E. lacei
Fig. 2C
sect.
Euphorbia
Old World
Clade II
(in part)
Habit
Leafy Tree/Shrub
Herb
Geophyte
Spiny xerophyte shrubs
Pencil-stem
Green-stem succulent
Distribution
Madagascar
Africa / Arabia
Asia
N. America
C. / S. America
Caribbean
P S. Pacific
To Fig. 2B
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
the New World sections are very short relative to those that
subtend each of them, and accordingly there is poor resolution
of the sectional relationships within the New World clade. As
with the backbone of the subgenus, this pattern is the same
as that found by Horn & al. (2012) in their species-poor but
marker-intensive phylogeny; thus this pattern is not likely to
be an artifact of taxon sampling or marker choice, but rather a
reflection of the history of this group. The New World clade is
where our results differ most from previous work. Five of the
eleven sections that we recognize here have been previously
described and remain largely unchanged in our circumscription, but the remaining six are new sections or are significant
recircumscriptions of previously named groups reflecting our
phylogenetic results.
A notable section we recognize among the New World species is E. sect. Euphorbiastrum, which is circumscribed here as
an unusually diverse group of species in terms of their growth
forms. At the base of this clade are two species, E. laurifolia
and E. cestrifolia, which are both small trees that occur in
open, dry scrubland in the northern to central Andes. The next
diverging species is E. weberbaueri, which is very different
from the previous two in being a semi-succulent pencil-stem
shrub growing in cactus-scrub vegetation of Peru and Ecuador. This is followed by E. dussii, which is a rare shrub from
moist forests of Martinique and St. Lucia in the Lesser Antilles.
Steinmann & al. (2007) hypothesized that E. dussii was part
of E. sect. Cubanthus, but our data place it instead well nested
within E. sect. Euphorbiastrum. This indicates that E. dussii
and E. sect. Cubanthus represent two separate introductions
of E. subg. Euphorbia into the West Indies. Euphorbia pteroneura is another semi-succulent species in this clade, with
green stems resembling those of E. weberbaueri, but it is an
herb from southern Mexico with fully developed, droughtdeciduous leaves. Sister to E. pteroneura is E. hoffmanniana,
a large shrub from Costa Rica. Despite the heterogeneous morphology of these species, their monophyly is highly supported
by our molecular sequence data (BS 93%; Fig. 2A). The relationship of this clade to other species in the New World clade,
however, has very little support. This section is a fine-scale
example of the lability of growth form evolution in Euphorbia
and of the potential this group holds for studying the drivers
of such evolutionary patterns.
Euphorbia sect. Pacificae (= Pacific clade). — This clade
was originally recovered by Steinmann and Porter (Steinmann
& Porter, 2002), although they only included three species.
Based on our results (Fig. 2A) as well as previous treatments
(Hassall, 1977; Forster, 1994), E. sect. Pacificae consists of
twelve species. Nine of these species form a complex related
to E. plumerioides, and are all shrubs to small trees that grow
in highland forests or coastal headlands in the southwestern
Pacific area, New Guinea, and tropical Australia. Three other
subtropical Australian species are included in E. sect. Pacificae,
namely E. boophthona, E. stevenii (both herbs), and E. sarcostemmoides (a pencil-stem shrub). Zimmermann & al. (2010)
included two accessions of E. boophthona in their analysis, one
from Steinmann & Porter (2002) and another from their own
collection. Their collection was placed in E. subg. Chamaesyce,
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TAXON 62 (2) • April 2013: 291–315
while the Steinmann collection was placed in E. sect. Pacificae.
Our own third accession is strongly supported as part of E. sect.
Pacificae and thus confirms the results of Steinmann & Porter
(2002) and Horn & al. (2012). This species is distinct from all
other members of E. sect. Pacificae in having four cyathial
glands and seeds with a pronounced caruncle, while the rest
of the species have five glands and ecarunculate seeds. The
cpDNA and 3-gene datasets resolve E. sect. Pacificae as sister
to the New World clade, but the ITS data place it sister to Old
World clade I. Both relationships have poor BS (≤ 55%), but
the clade itself is highly supported in all analyses regardless
of taxon sampling or sequence data used (BS 100%, PP > 95;
Fig. 2; Electr. Suppl.: Figs. S1–S3). Euphorbia sect. Pacificae
has a unique geographic distribution within Euphorbia (Fig. 2),
occurring mainly in Papua New Guinea and Australia but also
on islands of Malesia, the Philippines, Melanesia, and Hawaii.
Old World clade I. — The third major clade recovered in
our study, which we refer to as Old World clade I, is distributed mainly across Madagascar, but with several species in
Africa and the Arabian Peninsula. In the 3-gene and cpDNA
analyses (Fig. 2B; Electr. Suppl.: Fig. S2), this clade is sister
to the remaining Old World species, although in the ITS tree
it is sister to the Pacific clade (Electr. Suppl.: Fig. S1). Neither
of these placements is strongly supported, but the geographical distribution of Old World clade I supports the results of
our combined analyses (Fig. 2B). The exclusion of this group,
with high support (BS 100%), from the rest of the Madagascan
species (mostly placed in Old World clade II) suggests that
there have been at least two, and possibly three, independent
introductions to Madagascar within E. subg. Euphorbia.
Old World clade I contains several growth forms and a
diversity of cyathium and fruit characters, but it can be distinguished from other clades by the prevalence of dioecy in most
species. This reproductive system has not been conclusively
documented in all species, but it appears to be a morphological
synapomorphy for the clade. We recognize two sections in Old
World clade I, the newly described E. sect. Pervilleanae and
the substantially recircumbscribed E. sect. Tirucalli. Euphorbia
sect. Tirucalli, as circumscribed here, includes only pencilstemmed species that have photosynthetic, semi-succulent
branches that are typically long relative to their diameter and
usually bear rudimentary, caducous leaves (Fig. 1F) (Horn
& al., 2012). This growth form is exemplified by E. tirucalli, the
milkbush tree, which is commonly planted in the tropics but is
likely native to southern Africa or Madagascar. Euphorbia tirucalli has been the basis for a group at various ranks that has included all or most of the pencil-stemmed species in Euphorbia.
Previous work has shown that this was an artificial grouping
and that the pencil-stemmed habit has evolved independently
multiple times, and in each subgenus of Euphorbia (Steinmann
& Porter, 2002). The true relatives of E. tirucalli are a group
of 23 species occurring mostly in Madagascar, but with several species in Africa and the Arabian Peninsula (Fig. 2). The
various groups of pencil-stemmed species in Euphorbia are
often difficult to distinguish morphologically. In contrast, the
species of E. sect. Tirucalli are well-characterized as dioecious shrubs or trees, with alternate branches that can appear
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
whorled, conspicuous pubescence (especially on the ovaries),
female flowers with calyx lobes, and carunculate seeds. This
combination of characters can usually serve to tell all species
of E. sect. Tirucalli from pencil-stemmed species belonging
to other clades.
Old World clade II. — The remaining Old World species
in E. subg. Euphorbia comprise Old World clade II, which is
divided into four sections. The size of these sections varies
from over 350 species in E. sect. Euphorbia to three species in
E. sect. Rubellae. Species in Old World clade II are distributed
in Africa, Asia, and Madagascar, with the majority occurring
in warm, arid climates. Spines of various form, but generally
considered of stipular origin (White & al., 1941), are quite common in this clade, as are succulent stems (Fig. 1C, G, M–P).
Growth forms also vary greatly among the sections of Old
World clade II and include geophytes, pencil-stemmed shrubs
and trees, leafy shrubs and trees, spiny xerophytic shrubs, and
various kinds of stem succulents (Figs. 1B–E, M, 2B, C).
Support for Old World clade II and for each of the four
subclades is high (BS 100%, PP 1.0). However, only the cpDNA
analysis resolved the relationships among the subclades with
good support (BS > 80%; Electr. Suppl.: Fig. S2). Several nodes
differ between the ITS tree and the cpDNA tree (though with
low BS from ITS), and these are likely the cause of the low BS
support in the 3-gene tree. First, E. sect. Rubellae is inferred
as sister to the rest of Old World clade II in the ITS tree (Electr.
Suppl.: Fig. S1), but as sister to E. sect. Monadenium + E. sect.
Euphorbia in the cpDNA tree (Electr. Suppl.: Fig. S2). Second,
the sister clade of E. sect. Euphorbia is the clade of sections
Denisophorbia, Deuterocalli, and Goniostema in the ITS tree,
but it is E. sect. Monadenium in the cpDNA tree. Horn & al.
(2012), who compiled the largest dataset in terms of sequence
data, found the same sister relationship for E. sect. Euphorbia
as in our 3-gene tree (Fig. 2). However, they did not include
E. sect. Rubellae, so we cannot make comparisons about the
overall topology of Old World clade II. For simplicity, we discuss the groups within Old World clade II referring to the topology in Fig. 2.
Euphorbia sect. Rubellae, represented by E. rubella and
E. brunellii, is a group of three species from northeastern
Africa and is the only clade in E. subg. Euphorbia comprised
entirely of geophytic species. Aside from their habit, the most
distinctive feature of this group is the 4 + 2 arrangement of the
cyathial glands: four oblong-elliptic glands of equal size and
two smaller, orbicular ones that are apparently derived from
splitting of the original fifth gland (Gilbert, 1987). These species were formerly included in E. subg. Lacanthis (= E. sect.
Goniostema), but Haevermans & al. (2004) showed that the
species of E. sect. Rubellae are not part of E. sect. Goniostema,
which is now an entirely Madagascan group. Our results support their hypothesis of relationships.
Following E. sect. Rubellae in Old World clade II is a highly
supported clade (BS 100%) consisting of three sections endemic
to Madagascar: E. sect. Goniostema, E. sect. Denisophorbia,
and E. sect. Deuterocalli (Fig. 2B). In our ITS analysis, these
sections form monophyletic groups with 100% BS for E. sect.
Denisophorbia and sect. Deuterocalli, and low support (BS
56%) for E. sect. Goniostema (Electr. Suppl.: Fig. S1), but the
plastid data does not resolve the relationships of these three
groups well (Electr. Suppl.: Fig. S2). Consequently, E. sect.
Goniostema forms a grade in the 3-gene analysis, although
the other two sections are monophyletic and still have 100%
BS (Fig. 2B). The grade pattern of E. sect. Goniostema in the
3-gene analysis (Fig. 2B) is due to the placement of several
species (E. iharanae, E. neohumbertii, E. alfredii, E. geroldii,
E. francosii and E. viguieri) outside the core of E. sect. Goniostema in the analysis of the plastid dataset (Electr. Suppl.: Fig.
S2). Horn & al. (2012) included E. iharanae and E. neohumbertii
in their analysis and also found these two species to form a
clade outside the core of E. sect. Goniostema. Euphorbia iharanae and E. neohumbertii represent a group of species from
northern Madagascar that share the well-developed, colorful
cyathophylls of the rest of E. sect. Goniostema. Several species
in this northern group are unarmed trees or small shrubs from
the rainforest of northeastern Madagascar (e.g., E. geroldii),
while others are succulent shrubs or monocauls that occur in
dry habitats of northern Madagascar. The latter group has bristly
spines (e.g., E. viguieri, E. iharanae) or small glandular combs
(e.g., E. alfredii) in vertical rows along the stem (Fig. 1M). Some
are also distinguished by erect cyathophylls that envelop the
cyathia and resemble a floral tube (Fig. 1L). These species have
previously been placed in E. sect. Goniostema based on morphology and distribution, and despite their placement outside
the core of the section in our concatenated analyses, they are
part of a monophyletic E. sect. Goniostema in our ITS tree
(Electr. Suppl.: Fig. S1). Moreover, analyses by Aubriot (2012)
of two nuclear and six chloroplast regions, with comprehensive
sampling of E. sect. Deuterocalli, sect. Denisophorbia, and sect.
Goniostema, produce a well-resolved phylogeny that supports
the monophyly of the three sections in Old World clade II and
firmly places these species within E. sect. Goniostema.
One of the most morphologically distinct groups within
Old World clade II is E. sect. Monadenium, which is distributed
across eastern, central, and southern Africa. This is a highly
supported clade (BS 100%, Fig. 2B) of about 90 species that are
easily recognized morphologically by the fusion of the cyathial
glands into a horseshoe-shaped rim, or less commonly into a
complete ring. This unique cyathial morphology was the reason
this group was formerly segregated from Euphorbia, but our
results and those from previous studies have confirmed that this
section is well nested within E. subg. Euphorbia (Steinmann
& Porter, 2002; Bruyns & al., 2006; Zimmermann & al., 2010;
Horn & al., 2012). Species of E. sect. Monadenium are particularly diverse in terms of growth form and include geophytes,
succulent and non-succulent shrubs, as well as trees, vines, and
one pencil-stem species (Fig 2B).
The largest clade in E. subg. Euphorbia and perhaps the
best known is E. sect. Euphorbia—the “spine-shield” euphorbias (Fig. 1C, D, G, N). This group is a well-defined clade of
over 340 species distributed mostly in Africa but also across
southern and southeast Asia and into Indonesia. The defining character for this clade is the spine-shield—a horny pad
of tissue subtending or surrounding each leaf base that typically bears two or four spiny outgrowths (Fig. 1G, N). These
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
outgrowths are usually interpreted as a pair of stipular spines
and a pair of prickles (Carter, 1994). The vast majority of species in E. sect. Euphorbia have spine-shields, but they have
been lost in a few species, such as E. abdelkuri and E. piscidermis. Most species in this section are stem succulents that vary
in size from prostrate dwarf shrubs to large candelabriform
trees, and have angled, winged, or tuberculate stems and minute, caducous leaves. However, there are also geophytes and
large trees that have well developed leaves. Several geophytic
species from India, including E. fusiformis, E. nana (Fig. 1D),
and E. meenae, are now known to belong to E. sect. Euphorbia. There are no obvious characters placing them in E. sect.
Euphorbia because they lack above-ground stems. However,
DNA sequence data from previous studies confirm that they are
indeed part of this section (Steinmann & Porter, 2002; Bruyns
& al., 2006; Zimmermann & al., 2010).
Growth form evolution. — Euphorbia subg. Euphorbia
contains the full range of growth form diversity that is present
within the genus (Figs. 1A–F, 2). Moreover, our phylogenetic
results confirm the conclusion of Horn & al. (2012) that specialized growth forms have evolved independently, and repeatedly,
within the subgenus. Horn & al. (2012) inferred the common
ancestor of E. subg. Euphorbia to be a shrub or tree with alternate leaves and terminal cyathia. This growth form (exclusive
of the cyathial position) is mostly retained in E. sect. Pachysanthae, sect. Pervilleanae, and sect. Denisophorbia in Madagascar, as well as in most sections of the New World clade. The
herbaceous habit has evolved four times in E. subg. Euphorbia:
in the clade of E. sect. Portulacastrum + E. sect. Nummulariopsis, in E. pteroneura of E. sect. Euphorbiastrum, in E. sect.
Monadenium, and in several members of E. sect. Pacificae.
Geophytic species are present in all sections of Old World clade
II and comprise the entire E. sect. Rubellae. The one geophyte
from E. sect. Monadenium in our study, E. neogracilis, is sister
to the rest of the section in our cpDNA and 3-gene analyses.
The geophytes in E. sect. Goniostema and E. sect. Euphorbia
have been shown to be well nested within those clades. The
phylogenetic position of these geophytic species suggests that
geophytes have evolved independently multiple times in Old
World clade II (Haevermans & al., 2004; Zimmermann & al.,
2010; Bruyns & al., 2011). Similarly, the pencil-stem tree/shrub
habit appears to have evolved at least eight times in E. subg.
Euphorbia: four times in the New World clade, twice in Old
World clade I, and twice in Old World clade II (Fig. 2).
Highly succulent, photosynthetic stems are present in
E. sect. Euphorbia and in E. sect. Monadenium. While both of
these sections contain a range of growth forms, all but a few
species in E. sect. Euphorbia have spiny, succulent stems. The
exceptions include the geophytes mentioned above, and some
leafy trees such as E. drupifera. Species range from trees up to
25 m tall, such as E. cussonioides, to dwarf shrubs only a few
centimeters high, such as E. decidua. While most species have
minute, caducous leaves, some produce quite large, persistent
ones (e.g., E. neriifolia and E. royleana from India). Because
these species are nested well within E. sect. Euphorbia, the
presence of persistent leaves appears to be a reversal to the
ancestral state for the subgenus (Horn & al., 2012). Growth
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form evolution in E. sect. Monadenium involves changes in
habits rather than changes in size. This section contains the
entire range of growth forms found in the subgenus, and the
stem succulent species make up only a few of the total. While
the stems of some species are succulent and green, the loss of
functional leaves is much less pronounced in E. sect. Monadenium, and most species produce large, succulent leaves.
The switch to stem-based photosynthesis, as has happened
in E. sect. Euphorbia and in all pencil-stemmed species, putatively involves several steps, including an increase in the stem
stomatal density, delaying or abandoning bark initiation, increasing the volume of cortex for water storage, and the development of the Crassulacean Acid Metabolism (CAM) photosynthetic system (Nobel, 1988; Edwards & Donoghue, 2006).
Given the frequency with which stem-based photosynthesis
has evolved in E. subg. Euphorbia (Fig. 2), it seems that these
are relatively “easy” evolutionary transitions to make in this
group. In Cactaceae, Edwards & Donoghue (2006) showed
that Pereskia Mill. species, which are the closest relatives to
the core cacti, have high water use efficiency and some level of
CAM photosynthesis. They suggested that this was preadaptive
for the transition to the succulent-stemmed cactus life form.
CAM has been inferred in most stem photosynthetic species in
E. subg. Euphorbia, but the close relatives of the pencil-stem
species are all C3 plants (Horn & al., 2011), suggesting that
CAM is not a prerequisite for the evolution of highly succulent,
photosynthetic stems.
Diversity of cyathial morphology. — While most species
in E. subg. Euphorbia have relatively unspecialized radially
symmetric cyathia (with five, usually yellow glands that lack
appendages, and with small, inconspicuous cyathophylls),
some of the showiest and morphologically most derived forms
of cyathia in the genus are also found within this subgenus
(Fig. 1G–L). For example, all species in E. sect. Monadenium
possess cyathia with nectar glands fused either into a horseshoe
shape or a full circle, as well as cyathophylls that are more or
less fused dorsally, resulting in bilateral symmetry (Fig. 1J).
Euphorbia sect. Crepidaria contains another striking example of fusion of cyathial parts and a shift to bilateral symmetry (Fig. 1I). In this section, the nectar glands are positioned
on one side of the involucre and are enveloped in a spur formed
by the fusion of petaloid gland appendages. This is perhaps the
greatest deviation from the general form of the open, actinomorphic cyathium that resembles a typical dicot flower (Fig. 1G).
This cyathial form in E. sect. Crepidaria is often associated
with hummingbird pollination (Dressler, 1957) and represents
a unique syndrome within Euphorbia. Cacho & al. (2010) suggested that the nectar spur was a key innovation that led to a
rapid radiation in E. sect. Crepidaria. They noted that high
morphological divergence relative to the low sequence variation
among species suggested a rapid radiation after the evolution of
nectar spurs, especially when coupled with the long branch leading to the extant members of the clade (found in our study and
Bruyns & al., 2006, 2011; Zimmermann & al., 2010). However,
they were unable to find unique support for the key innovation
hypothesis except when assuming an outgroup of only one species. Our results do not resolve the sister relationship of E. sect.
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
Crepidaria, but place it most closely to clades that would also
be unlikely to support the key innovation hypothesis.
Well-developed cyathophylls occur in E. sect. Goniostema, and this is a morphological synapomorphy for the clade
(Fig. 1H). Most species in E. sect. Goniostema have cyathophylls that become brightly colored (usually red or yellow)
and can be spreading, or in a few species (e.g., E. neohumbertii, E. iharanae) envelop the cyathium completely, mimicking a pseudofloral tube (Fig. 1L). Effects on pollination are
unknown, but the change in shape in these “tubular” cyathia
presumably affects the mechanism and/or effort required to
access the nectar and could be associated with more specialized pollinators.
CONCLUSIONS
This study represents the most taxonomically and geographically comprehensive phylogenetic study of Euphorbia
subg. Euphorbia to date. Sequence data from multiple regions
representing the nuclear and plastid genomes allowed us to infer
phylogenetic relationships across the subgenus, and they support four major lineages within the subgenus that can be characterized by their distributions. Our results clearly establish the
monophyly of all New World species in E. subg. Euphorbia,
define the species composition of the New World clade, and
suggest a split between the Old World and New World early in
the history of the subgenus. Our phylogeny also supports the
hypothesis of at least two independent lineages in Madagascar
within E. subg. Euphorbia. Included in these is E. sect. Tirucalli, which is recircumbscribed as the clade of pencil-stemmed
species within E. subg. Euphorbia that includes E. tirucalli.
Also included in these Madagascan clades are three sections of
leafy shrubs and trees (E. sect. Denisophorbia, E. sect. Pervilleanae, E. sect. Pachysanthae) that will require more thorough
study to better understand their circumscriptions and the delimitations of species within them.
Consistent with the overall evolutionary lability of growth
form in Euphorbia as a whole, several of the sections in E. subg.
Euphorbia contain a wide range of growth forms for their small
size. The pencil-stem growth form is particularly homoplasious
within the subgenus, just as it is across the genus as a whole.
Utilizing the phylogenetic framework established in this study,
future studies will focus on potential drivers of the evolution
of the unusual pencil-stem growth form as well as patterns of
geographical and morphological differentiation in the large
spine-shield clade, E. sect. Euphorbia.
database of names and synonyms with additional information
is available online at the Tolkin website (http://app.tolkin.org/
projects/72/taxa, Riina & Berry, 2012).
Euphorbia L., Sp. Pl.: 450. 1753 – Type (designated by Millspaugh in Publ. Field Columb. Mus., Bot. Ser. 2: 306. 1909):
Euphorbia antiquorum L.
Euphorbia L. subg. Euphorbia ≡ Euphorbia subg. Tithymalus
Pers., Syn. Pl. 2(1): 10. 1806.
As the largest and most diverse of the four subgenera of
Euphorbia, E. subg. Euphorbia is probably the most difficult to
characterize morphologically. This clade has the greatest number of succulent and spiny species. Euphorbia subg. Athymalus
also has a significant number of spiny, succulent species, but
the spines in that group are generally of peduncular origin,
whereas in E. subg. Euphorbia they are either stem enations
or more complex “spine-shields” that may be of stipular origin
(Fig. 1M–P) (Carter, 1994). Many of the succulent, spiny species are leafless, but members of both E. sect. Euphorbia and
sect. Goniostema can also be both leafy and spiny. There are
a number of evergreen or deciduous tree species in E. subg.
Euphorbia in both Madagascar and the New World, and there
are several lineages or species that show leafless and spineless
pencil-stem habits. There are rather few truly herbaceous species in the subgenus, and a limited number of geophytes occur
in at least four Old World clades.
Reproductively, E. subg. Euphorbia is notable for its wide
variations of the cyathium, particularly in gland number,
shape, and degree of fusion (Fig. 1G–L). The glands generally lack appendages, but there are several small groups with
short horns (Fig. 1K), finely divided rims, or even finger-like
processes. The bracts immediately subtending the cyathia, as
opposed to the dichasial bracts subtending or along the rays
of the synflorescence, are showy and diagnostic in several
groups (Fig. 1H, L). In our descriptions below we use the term
“cyathophylls” to refer to these subcyathial bracts in all groups.
The larger sections have bisexual cyathia, but dioecy is characteristic of some of the smaller sections. Similarly, caruncles
are present in some groups, but absent in others.
Although certain sections of E. subg. Euphorbia can be
readily distinguished by their specialized cyathial features (e.g.,
E. sect. Crepidaria and E. sect. Monadenium), many sections
have a similar, basic cyathium, and habit types have been shown
to be particularly homoplasious in the subgenus. This makes
construction of a morphologically based key to the sections problematic; however, since major clades in the subgenus are well circumscribed geographically, the most straightforward approach is
to first break the subgenus into these more manageable groups.
TAXONOMIC TREATMENT
Altogether, 661 species are recognized in the subgenus. For
each section listed below, we provide a list of their component
species. Those species appearing in boldface-italics have been
sampled molecularly in this or in previous studies, whereas
those appearing only in italics are inferred to belong to the
section based on their morphology and distribution. A complete
Key to the sections of Euphorbia subg. Euphorbia
1
1
2
2
Old World natives ......................................... 2
New World natives ....................................... 13
Madagascar and Indian Ocean islands .................. 3
Other Old World and Pacific areas outside of Madagascar
and the Indian Ocean ..................................... 9
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Stipules spiny, papyraceous or comb-like, more or less
branched, diversely colored; cyathia always bisexual;
cyathophylls well developed (except E. boissieri); seeds
verrucose; caruncle absent .... E. sect. Goniostema (17)
3 Stipules glandular or punctiform, never spiny or papyraceous; cyathia unisexual or bisexual; cyathophylls developed or reduced; seeds smooth; caruncle present or
absent ...................................................... 4
4 Plants essentially leafless (leaves very small, soon caducous); young stems succulent and photosynthetic ...... 5
4 Plants with well-developed leaves, caducous or persistent;
young stems not succulent or photosynthetic ........... 7
5 Reduced leaves when present more or less lanceolate; petiole base surrounded by a glandular or waxy ring (possibly
of stipular origin, but clearly visible after the leaves have
fallen off) ...................... E. sect. Deuterocalli (18)
5 Reduced leaves when present variable in shape, but not
lanceolate; stipules extremely reduced, located on each
side of the leaf insertion (visible or not after the leaves
have fallen off) ............................................ 6
6 Twigs glabrous; synflorescences terminal; female flower
without a calyx; capsule 1- or 2-locular; seeds wider than
long, ecarunculate .. E. sect. Pervilleanae (14) (E. intisy)
6 Young twigs more or less tomentose; synflorescences subterminal; female flower with a rudimentary calyx; capsule
3-locular; seeds longer than wide, with a well-developed
caruncle ................... E. sect. Tirucalli (in part) (15)
7 Shrubs or trees with sympodial branching, the leaves clustered at nodes connected by slender leafless shoots; cyathia
unisexual (rarely bisexual); capsule 3-locular, smooth;
seeds cylindrical, smooth ... E. sect. Denisophorbia (19)
7 Shrubs or trees with monopodial growth, the leaves regularly spaced or else clustered at the twig apex; cyathia
bisexual; capsule 1-or 2-locular, ornamented or not; seeds
globose, smooth or sculptured ........................... 8
8 Shrubs or trees with thick coriaceous leaves; cyathium
shallowly bowl-shaped, with large stipitate glands (> 5 mm
wide); fascicles of male flowers sheathed by their bracteoles; capsule erect, apparently largely indehiscent, more
or less fleshy, the surface smooth or wrinkled, seeds 1
or 2 ............................. E. sect. Pachysanthae (13)
8 Shrubs or trees with soft and thin leaves; cyathium cupshaped with sessile glands; male flowers not sheathed by
their bracteoles; capsule pendulous, dehiscent, winged or
with spiny appendages, seeds usually 2 ...................
.................................... E. sect. Pervilleanae (14)
9 Natives of Australia and Pacific Islands including New
Guinea .............................. E. sect. Pacificae (1)
9 Natives of Africa, Arabia, and Asia .................... 10
10 Plants mostly dioecious, essentially leafless (leaves very
small, soon caducous), pencil-stemmed shrubs or trees;
young stems succulent and photosynthetic, usually terete,
more or less tomentose, spines absent ....................
.............................. E. sect. Tirucalli (in part) (15)
10 Plants monoecious geophytes, shrubs, or trees either with
well developed, caducous or persistent leaves and nonphotosynthetic stems, or else leafless and succulent with
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3
304
11
11
12
12
13
13
14
14
15
15
16
16
17
17
18
18
19
19
20
20
21
photosynthetic stems, but then usually with spine-shields
or stipular spines ......................................... 11
Geophytes with free cyathophylls and cyathia with 4 similar glands and a fifth one divided into two parts; seeds
carunculate; northeast Africa ..... E. sect. Rubellae (16)
Plants varied in habit, but if geophytic then with glands
fused into a horseshoe shape and with carunculate seeds,
or else with highly reduced cyathophylls, 5 similar glands,
and ecarunculate seeds; widespread (Africa, southern/eastern Asia) .................................................. 12
Stems spineless or with spines of stipular origin, but no
spine-shields; cyathophylls usually (partly) fused on one
side; cyathia with one large horseshoe-shaped or circular
gland; seeds carunculate .... E. sect. Monadenium (20)
Stems usually succulent, angled or tuberculate, generally
with distinctive spine-shields composed of a horny pad
and associated spines; cyathophylls reduced, scale-like;
cyathia actinomorphic, with 5 similar glands; seeds ecarunculate ......................... E. sect. Euphorbia (21)
Cyathia strongly zygomorphic, the glands hidden in a spurlike extension of the cyathial involucre ...................
...................................... E. sect. Crepidaria (10)
Cyathia actinomorphic, or if slightly zygomorphic, the
glands evident on the surface or edge of the involucre . 14
Leafless stem-succulent shrubs, stems with 4–6 angles or
ridges ...................................................... 15
Leafy herbs, shrubs, or trees (sometimes deciduous), stems
terete or rarely angled ................................... 16
Cyathial glands with two horns; eastern Brazil ..........
.................................... E. sect. Brasilienses (12)
Cyathial glands without horns; Ecuador and Peru .......
........... E. sect. Euphorbiastrum (6) (E. weberbaueri)
Cyathia arranged in a tight synflorescence with the subtending bracts greenish and successively overlapping each
other like shrimp scales ....... E. sect. Stachydium (11)
Cyathia laxer and not subtended by overlapping greenish
bracts ...................................................... 17
Herbs ...................................................... 18
Shrubs or trees ........................................... 20
Annuals, the petioles longer than the blades; cyathia solitary and axillary, the glands each with 3–5 digitate appendages ........................... E. sect. Portulacastrum (8)
Perennials, the petioles generally shorter than the blades;
cyathia in dichasia or pleiochasia, the glands without
appendages or else with two horns ..................... 19
Stems terete; pistillate flowers with evident perianth lobes;
southern South America and southeastern United States
................................ E. sect. Nummulariopsis (9)
Stems ridged; pistillate flowers without evident perianth
lobes; Mexico and Guatemala .............................
.................. E. sect. Euphorbiastrum (E. pteroneura)
Shrubs to small trees of moist evergreen tropical forests;
leaves very large, 25–40 × 5–12 cm, persistent ..........
..................................... E. sect. Mesophyllae (5)
Shrubs or trees of drier, more subtropical habitats; leaves
smaller than above, persistent or deciduous ........... 21
Densely branched bushes; cyathia subtended by numerous
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22
22
23
23
24
24
Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
(4–6) creamy-yellow, leafy cyathophylls; edge of Atacama
Desert in northern Chile ......... E. sect. Lactifluae (4)
Laxly branched shrubs or single-trunked trees; cyathia
usually subtended by 2 or 3 cyathophylls; from Andean
Peru north to Mexico and the Caribbean .............. 22
Cyathophylls red (green in E. cubensis); cyathial glands
1–8, on the rim of the involucre or on its outer wall; Caribbean islands (Bahamas, Hispaniola, Cuba, Jamaica) ....
...................................... E. sect. Cubanthus (3)
Cyathophylls, when present, whitish or yellowish; cyathial
glands 4 or 5, on the rim of the involucre; Mexico to Peru
(one species, E. dussii, from St. Lucia in the Caribbean)
.............................................................. 23
Shrubs or small trees to ca. 5 m tall; cyathia subtended
by greenish or inconspicuous cyathophylls; Costa Rica to
Peru and St. Lucia (Caribbean) ............................
................................ E. sect. Euphorbiastrum (6)
Small to large trees 5–25 m tall; cyathia subtended by 2 or
3 whitish or yellowish cyathophylls; Mexico .......... 24
Trees to 12 m tall with rugose to furrowed bark; capsule
exserted from the involucre, seeds carunculate ..........
...................................... E. sect. Calyculatae (7)
Trees to 25 m tall with coppery, exfoliating bark; capsule
included within or barely exserted from the involucre,
seeds ecarunculate ............. E. sect. Tanquahuete (2)
1. Euphorbia sect. Pacificae Dorsey, sect. nov. – Type: Euphorbia plumerioides Teijsm. ex Hassk.
Monoecious or dioecious herbs, shrubs, or small trees.
Stems woody to fleshy, terete, glabrous. Stem leaves alternate,
those on fertile branches opposite in E. boophthona, persistent
to caducous, thin to fleshy, usually petiolate; stipules absent.
Synflorescences subterminal, much-branched dichasia or solitary, axillary cyathia; cyathia pedunculate; glands (4)5(–11),
green, ovate-elliptic, with short marginal processes. Capsule
(sub)globose; seeds oblong to ovoid (cylindrical in E. boophthona), carunculate (E. boophthona) or ecarunculate.
Species included (11). – E. boophthona C.A. Gardner,
E. brassii P.I. Forst., E. buxoides Radcl.-Sm., E. haeleeleana
Herpst, E. heyligersiana P.I. Forst., E. indistincta P.I. Forst.,
E. kanalensis Boiss., E. norfolkiana Boiss., E. plumerioides
Teijsm. ex Hassk., E. sarcostemmoides J.H. Willis, E. stevenii
F.M. Bailey.
Distribution and habitat. – Australia, Indonesia, New
Guinea, Philippines, and Pacific Islands (Norfolk Island, Fiji,
Solomon Islands, Hawaiian Islands); the Australian herbaceous
or pencil-stemmed species occur in dry interior or coastal habitats, whereas the remaining species occur in tropical or subtropical moist forests or scrub.
Euphorbia sect. Pacificae is a novel grouping that has a
unique southern Pacific distribution within Euphorbia. It contains the E. plumerioides complex (Forster, 1994), a group of
eight or nine shrubby species, which is most diverse in New
Guinea. Whether E. euonymoclada Croizat belongs here or
not is uncertain and will require obtaining molecular data
and more specimens of this rarely collected species; it differs from the other members of the E. plumerioides complex
in its well-developed stipules and single-cyathiate synflorescence. Three quite different-looking species that are endemic
to Australia are also included in E. sect. Pacificae, namely
E. boophthona, E. stevenii, and E. sarcostemmoides. The first
two are herbs, whereas E. sarcostemmoides is a leafless pencilstemmed shrub. Euphorbia boophthona is morphologically
anomalous here, since it has four cyathial glands and seeds
with a pronounced caruncle. An unusual species belonging to
this group is E. haeleeleana, which is endemic to Kauai and
Oahu in the Hawaiian Islands; it is a tree with large, woody
fruits and cyathia with up to 11 glands.
2. Euphorbia sect. Tanquahuete V.W. Steinm. & Dorsey, sect.
nov. – Type: Euphorbia tanquahuete Sessé & Moc.
Trees to 25 m tall, trunk to 50 cm d.b.h. Stems round in
cross-section, glabrous to pubescent, bark smooth and exfoliating into thin papery sheets. Leaves spirally arranged, droughtdeciduous; stipules glandular, minute, lateral at the base of the
petiole; petiole well-defined; blade elliptic, base attenuate, apex
acute, obtuse, mucronulate or apiculate, margin entire, glabrous
to pubescent, pinnately nerved. Synflorescence axillary, originating from leafless nodes of older stems, rays 3–9, dichasia
1-branched; cyathophylls 2, white to yellow; involucres on a
thick peduncle that becomes woody in fruit; glands 5, patelliform, situated on the rim of the involucre, without appendages;
gynophore terminating in 3 short triangular calyx-like lobes;
ovary glabrous, styles connate at the base, shortly swollenclavate, apex inconspicuously bifid to lobed. Capsule included
within or barely exserted from the involucre, dry or with a
slightly fleshy mesocarp; seeds broadly ovoid to subglobose,
rounded to slightly quadrangular in cross-section, base and
apex rounded, smooth, ecarunculate.
Distribution and habitat. – Central-western to southern
Mexico; subtropical deciduous forests in montane canyons and
lava flows; near sea level to 2100 m.
Species included (2). – E. lundelliana Croizat, E. tanquahuete Sessé & Moc.
Euphorbia sect. Tanquahuete contains two tree species that
are by far the largest members of Euphorbia in the New World,
and among the largest in the genus. Euphorbia lundelliana is
poorly known, but is placed here because of its arborescent
habit, leaves similar to E. tanquahuete, large fruits, and smooth,
ecarunculate seeds.
3. Euphorbia sect. Cubanthus (Boiss.) V.W. Steinm. & P.E.
Berry in Anales Jard. Bot. Madrid 64: 123–133. 2007 ≡
Pedilanthus sect. Cubanthus Boiss. in Candolle, Prodr.
15(2): 7. 1862 ≡ Cubanthus (Boiss.) Millsp. in Publ. Field
Mus. Nat. Hist., Bot. Ser. 2: 371. 1913 – Type: Pedilanthus
linearifolius Griseb. (≡ Euphorbia scutiformis V.W. Steinm.
& P.E. Berry).
= Adenorima Raf., Fl. Tellur. 4: 112. 1838 (‘1836’) ≡ Euphorbia
sect. Adenorima (Raf.) G.L. Webster in J. Arnold Arbor.
48: 407. 1967 – Type: Adenorima punicea (Sw.) Raf. (≡
Euphorbia punicea Sw.).
Monoecious shrubs to small trees; stems soft-wooded,
somewhat fleshy, terete. Leaves alternate, spirally arranged,
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
clustered toward branch apices, membranaceous to slightly
coriaceous, entire, sessile; stipules minute, glanduliform, caducous or apparently absent. Cyathia in terminal dichasia;
cyathophylls generally red; glands 1–8, situated on the rim
of the involucre or on its outer wall, green, yellow or reddish,
appendages lacking; ovary and fruit smooth, glabrous, usually subtended by a three-lobed, calyx-like structure; seeds
ecarunculate.
Euphorbia sect. Cubanthus is the only section within
E. subg. Euphorbia with a strictly Caribbean distribution. The
cyathial glands are distinctive in E. subsect. Moa in being usually placed on the outer wall of the involucre (rather than on
the rim) and in three species, E. millspaughii, E. scutiformis,
and E. umbelliformis, reduced to a single gland.
3a. Euphorbia subsect. Cubanthus V.W. Steinm. & P.E. Berry
in Anales Jard. Bot. Madrid 64: 123–133. 2007 – Type:
Pedilanthus linearifolius Griseb. (≡ Euphorbia scutiformis
V.W. Steinm. & P.E. Berry).
Leaves narrowly spathulate, clustered at branch apices,
those subtending the cyathia not distinct; cyathophylls red but
less intensely so than in E. subect. Moa (green in E. cubensis);
glands usually on the outer wall of the involucre.
Distribution and habitat. – Caribbean (Bahamas, Cuba,
Jamaica); scrub forest mostly on limestone, sea level to 500 m.
Species included (6). – E. cubensis Boiss., E. gymnonota
Urb., E. millspaughii V.M. Steinm. & P.E. Berry, E. punicea
Sw., E. scutiformis V.W. Steinm. & P.E. Berry, E. umbelliformis (Urb. & Ekman) V.W. Steinm. & P.E. Berry.
3b. Euphorbia subsect. Moa V.W. Steinm. & P.E. Berry in Anales Jard. Bot. Madrid 64: 123–133. 2007 – Type: Euphorbia
helenae Urb.
Leaves elliptic to oval, regularly spaced along stems, those
subtending the cyathia bright red and distinct in shape. Cyathophylls showy, red; involucre red; glands yellow, situated on involucre rim; male flowers red except for anthers; female flower red.
Distribution and habitat. – Caribbean (eastern Cuba);
scrub and forests on serpentine soils, sea level to 800 m.
Species included (3). – E. helenae Urb., E. munizii
Borhidi, E. podocarpifolia Urb.
4. Euphorbia sect. Lactifluae Dorsey & V.W. Steinm., sect.
nov. – Type: Euphorbia lactiflua Phil.
Xerophytic shrubs, to 2.5 m tall, but mostly 1 m or less,
soft-wooded and highly branched, bark grayish to red-brown,
not exfoliating, drought deciduous; stems rounded in crosssection; whole plant glabrous. Leaves well developed, spirally
arranged, loosely arranged on long shoots or highly congested
on short shoots; stipules absent or represented by minute punctiform glands less than 0.1 mm in diameter at the base of the
petiole; petiole short and inconspicuous; blade linear to narrowly elliptic, base attenuate, apex acute to apiculate, margin
entire, secondary venation not evident. Synflorescences terminal on short lateral shoots, sometimes terminal on main
branches; rays 3 or 4, dichasial bracts and cyathophylls showy,
numerous (3–6), pale yellow; cyathia 2(3), sessile, glands 5(6),
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transversely oblong, situated on the rim of the involucre, without appendages; gynophore terminating in 3 inconspicuous,
rounded calyx-like lobes; ovary glabrous, styles united into
a short column ca. 1/6 their length, apex emarginate to bifid.
Capsule barely exserted from the involucre; seeds plumply
obloid, rounded in cross-section, base and apex rounded,
smooth, with a conspicuous, hooded caruncle.
Distribution and habitat. – Northern Chile, rocky areas of
Atacama Desert from the region of Antofagasta south to the
vicinity of Copiapó; nearly sea level to 700 m.
Species included (1). – E. lactiflua Phil.
Euphorbia lactiflua is distinctive in its swollen branches
and showy, yellowish cyathophylls. Although it was previously
treated together with a number of leafless Old World succulents
in E. sect. Tirucalli Boiss. (Boissier, 1862), all molecular phylogenetic analyses show that E. sect. Lactifluae is an isolated
lineage within the New World clade of E. subg. Euphorbia.
5. Euphorbia sect. Mesophyllae V.W. Steinm. & Dorsey, sect.
nov. – Type: Euphorbia sinclairiana Benth.
Mesophytic shrubs or small trees to 5 m tall, littlebranched, bark not exfoliating. Stems thick and fleshy, rounded
in cross-section, glabrous. Leaves large (25–40 × 5–12 cm), obovate to oblanceolate, loosely and spirally arranged, pinnately
veined, margin entire; stipules well-developed, lateral at the
base of the petiole, ovate to triangular, caducous and leaving a
conspicuous calloused pad; petiole distinct, less than 1/10 the
length of blade. Synflorescence terminal (sometimes appearing
axillary), often long-pedunculate; cyathophylls 2, foliaceous
or scale-like and highly reduced; cyathia on short peduncles,
glands 5, circular to transversely oblong, situated on the rim
of the involucre, without appendages; gynophore terminating
in 3 triangular calyx-like lobes; ovary glabrous, styles united
into a slender column 4/5 to 5/6 their length, apex emarginate
to bifid. Capsule included within or barely exserted from the
involucre, deeply 3-lobed, smooth or reticulately ridged; seeds
globose to ovoid, rounded in cross-section, base truncate with
a circular depression, apex mucronulate, smooth, ecarunculate.
Distribution and habitat. – Mexico (Chiapas), Costa Rica,
Nicaragua, Panama, Colombia, Ecuador, Peru, Brazil (Acre),
Bolivia; understory of wet, lowland forests but also extending
to higher elevations in cloud forest, from near sea level to ca.
800 m.
Species included (1). – E. sinclairiana Benth.
Bernal & al. (2006) provided a discussion of the morphological variation within this species and concluded that
Euphorbia elata is best treated as a synonym of Euphorbia
sinclairiana. Three other species similar to E. sinclairiana
have been described (E. capansa Ducke, E. tessmannii Mansf.,
E. valerii Standl.). We treat them here as a single widespread
species that varies in characters such as inflorescence length
and persistence of the cyathophylls, but is characterized by the
extremely distinctive habit and large, oblanceolate leaves, as
well as growing in wet forest understorys.
6. Euphorbia sect. Euphorbiastrum (Klotzsch & Garcke) Boiss.
in Candolle, Prodr. 15(2): 10, 98. 1862 ≡ Euphorbiastrum
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
Klotzsch & Garcke in Monatsber. Königl. Preuss. Akad.
Wiss. Berlin 1859: 252. 1860 – Type (see Wheeler in Amer.
Midl. Naturalist 30: 467. 1943): Euphorbiastrum hoffmannianum Klotzsch & Garcke (≡ Euphorbia hoffmanniana
(Klotzsch & Garcke) Boiss.).
= Euphorbiodendron Millsp. in Publ. Field Columb. Mus., Bot.
Ser. 2: 305. 1909 – Type (see Wheeler in Amer. Midl. Naturalist 30: 467. 1943): Euphorbia laurifolia Juss.
= Euphorbia sect. Pteroneurae A. Berger, Sukkul. Euphorb.:
28. 1906 – Type: Euphorbia pteroneura A. Berger.
Herbs, shrubs or small trees; branches woody with bark or
else green and succulent (then without leaves or with only rudimentary ones, and stems 4–6-ridged). Leaves oblong to rhombic or scale-like and then caducous, stipules present (glandular
and surrounding the leaf scar) or absent. Synflorescences axillary or terminal, subsessile to pedunculate; cyathia subsessile
to pedunculate; glands 4 or 5, appendages lacking; cyathophylls
minute to longer than cyathium; seeds with a tiny caruncle.
Distribution and habitat. – Northern and central Andes
of South America (Venezuela, Colombia, Ecuador, Peru), to
southern Mexico and West Indies (Windward Islands); montane
scrub and forest edges, lowland moist forests.
Species included (6). – E. cestrifolia Kunth, E. dussii
Krug & Urb. ex Duss, E. hoffmanniana (Klotzsch & Garcke)
Boiss., E. laurifolia Juss. ex Lam., E. pteroneura A. Berger,
E. weberbaueri Mansf.
Multiple states from several morphological characters
are present in this section, and the group is not easily characterized morphologically. However, as noted in Steinmann
& Porter (2002), several morphological characters support the
close relationship of these species, including the carunculate
seeds and the well-developed, complex glandular stipules in
E. weberbaueri and E. cestrifolia.
7. Euphorbia sect. Calyculatae V.W. Steinm & Dorsey, sect.
nov. – Type: Euphorbia calyculata Kunth.
Trees or shrubs to 12 m tall, trunk to 20 cm d.b.h. Stems
round in cross-section, glabrous or sparsely pubescent, bark
rugose to furrowed. Leaves spirally arranged, loosely so
(E. xylopoda) or congested at the ends of the branches (E. calyculata), drought-deciduous; stipules present, glanduliform-conical,
lateral at the base of the petiole; blade elliptic, base attenuate,
apex acute or obtuse, margin entire, pinnately veined. Synflorescences subterminal with 3–5 rays and dichasia 2–4 times
branched (E. calyculata) or cyathia solitary and terminal at the
ends of the main branches and subtended by three prominent
white cyathophylls (E. xylopoda); cyathia pedunculate, glands 5,
transversely elliptic to oblong, situated on the rim of the involucre, without appendages; gynophore terminating in 3 triangular
calyx-like lobes; ovary glabrous, styles united into a column for
1/5 to 2/3 their length, swollen and emarginate at the apex. Capsule exserted from the involucre; seeds obloid, slightly angled
in cross-section, base and apex rounded, smooth, carunculate.
Distribution and habitat. – Mexico (Jalisco, Michoacán,
Guanajuato, Guerrero, Mexico, Oaxaca, Puebla); deciduous
montane woodlands, oak and pine-oak forest, sometimes on
lava flows, 1600–2300 m.
Species included (2). – E. calyculata Kunth, E. xylopoda
Greenm.
Euphorbia sect. Calyculatae contains two closely related
but morphologically very distinct species. Whereas E. calyculata has terminal pseudopleiochasial synflorescences typical
of many groups of Euphorbia, the cyathia of E. xylopoda are
solitary and terminal at the tips of the main branches, an uncommon condition in the genus. Steinmann & al. (2007) noted
morphological similarities between E. calyculata and E. sect.
Cubanthus, particularly in the leaf arrangement and calyx-like
structure, but a close relationship between these sections is not
supported by our data.
8. Euphorbia sect. Portulacastrum Boiss. in Candolle, Prodr.
15(2): 9, 69. 1862 – Type (see Wheeler in Amer. Midl.
Naturalist 30: 481. 1943): Euphorbia pentlandii Boiss.
Monoecious, annual, procumbent, pubescent herbs. Leaves
sparse, entire, ovate to orbicular, petioles as long as blade or
longer. Cyathia axillary, solitary, sessile or shortly pedunculate; glands 4, with appendages 3–5-digitate; styles undivided.
Capsule depressed ovoid, strongly 3-sulcate; seeds transversely
grooved, ecarunculate.
Distribution and habitat. – Bolivia and Chile; montane
habitats.
Species included (2). – E. germainii Boiss., E. pentlandii
Boiss.
This is a rarely collected section that differs from its sister
clade, E. sect. Nummulariopsis, in consisting of annual herbs
without pistillate calyces and with digitate cyathial gland
appendages.
9. Euphorbia sect. Nummulariopsis Boiss. in Candolle, Prodr.
15(2): 9, 71. 1862 – Type: Euphorbia peperomioides Boiss.
= Euphorbia subsect. Inundatae G.L. Webster in J. Arnold
Arbor. 48: 400. 1967 – Type: Euphorbia inundata Torr.
Monoecious or dioecious herbs, usually perennial, often
with a fleshy rootstock. Stems terete, ascending or prostrate.
Leaves alternate or sometimes opposite on vegetative stems,
entire to serrate, opposite on fertile rays, stipules glandular,
minute to elongate. Cyathia solitary and axillary or in terminal
pseudopleiochasia, glands 4–5(7), without appendages or sometimes 2-horned; female flower with well-developed perianth
lobes; ovary globose; seeds smooth to variously sculptured,
ecarunculate.
Distribution and habitat. – Southeastern U.S.A., southern South America (Argentina, Bolivia, Brazil, Chile, Paraguay, Peru, Uruguay); high montane habitats, grasslands, and
sand dunes (South America), pine woodlands and sandy areas
(U.S.A.), sea level to ca. 3500 m.
Species included (37). – E. araucana Phil., E. boerhaavioides Rusby, E. burkartii Bacigalupo, E. caespitosa Lam.,
E. chamaeclada Ule, E. copiapina Phil., E. cordeiroae P. Carrillo & V.W. Steinm., E. correntina Parodi, E. cymbiformis
Rusby, E. duriuscula Pax & K. Hoffm. ex Herzog, E. eanophylla Croizat, E. elodes Boiss., E. elquiensis Phil., E. floridana Chapm., E. guachanca Haenke in Azara, E. guaraniorum
P. Carrillo & V.W. Steinm., E. hieronymi Subils, E. hinkleyorum
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
I.M. Johnst., E. huanchahana (Klotzsch & Garcke) Boiss.,
E. inundata Torr. ex Chapm., E. macraulonia Phil., E. ovalleana Phil., E. pampeana Speg., E. papillosa A. St.-Hil., E. paranensis Dusén, E. pedersenii Subils, E. peperomioides Boiss.,
E. porphyrantha Phil., E. portulacoides L., E. raphanorrhiza
(Millsp.) J.F. Macbr., E. raphilippii Oudejans, E. rhabdodes
Boiss., E. rosescens E.L. Bridges & Orzell, E. schickendantzii
Hieron., E. stenophylla (Klotzsch & Garcke) Boiss., E. telephioides Chapm., E. thinophila Phil.
Most species in this section are confined to southern South
America, but a group of four species are disjunct to the southeastern United States and was formerly treated as E. subsect.
Inundatae G.L. Webster (Bridges & Orzell, 2002). Here this
group is strongly supported as sister to the South American
species. Both groups share the uncommon feature of a relatively
well-developed calyx on the female flower. The species from
the southeastern United States are functionally dioecious, a
feature so far shared only with E. hieronymi among the South
American species (Bridges & Orzell, 2002).
10. Euphorbia sect. Crepidaria (Haw.) Baill., Étude Euphorb.:
284. 1858 ≡ Crepidaria Haw., Syn. Pl. Succ.: 136. 1812 – Type
(see Wheeler in Contr. Gray Herb. 124: 44. 1939): Crepidaria
myrtifolia (Mill.) Haw. (= Euphorbia tithymaloides L.).
= Pedilanthus Neck. ex Poit., Elem. Bot. 2: 354. 1790 ≡ Tithymaloides sect. Pedilanthus M. Gómez, Fl. Habanera: 154.
1897 ≡ Tithymalus Mill., Gard. Dict. ed. 4, 3. 1754, nom.
rej. ≡ Tithymaloides Ortega, Tab. Bot.: 9. 1773, nom. rej. –
Type (Millspaugh in Publ. Field Columb. Mus., Bot. Ser.
2: 300. 1909): Pedilanthus tithymaloides (L.) Poiteau (≡
Euphorbia tithymaloides L.).
= Ventenatia Tratt., Gen. Pl.: 86. 1802 – Type: Ventenatia bracteata (Jacq.) Tratt. (≡ Euphorbia bracteata Jacq.).
= Diadenaria Klotzsch & Garcke in Monatsber. Königl. Preuss.
Akad. Wiss. Berlin 1859: 254. 1860 ≡ Tithymaloides sect.
Diadenaria (Klotzsch & Garcke) O. Kuntze in Post
& Kuntze, Lex. Gen. Phan.: 562. 1903 – Type (Wheeler
in Contr. Gray Herb. 124: 44. 1939): Diadenaria pavonis
Klotzsch & Garcke (= Euphorbia bracteata Jacq.).
= Hexadenia Klotzsch & Garcke, Monatsber. Königl. Preuss.
Akad. Wiss. Berlin 1859: 253. 1860 – Type: Hexadenia
macrocarpa (Benth.) Klotzsch & Garcke (≡ Euphorbia
lomelii V.W. Steinm.).
Monoecious shrubs to small trees. Stems succulent or not.
Leaves alternate, minute and scale-like to large and elliptic,
deciduous to persistent, entire; petiole short to absent, stipules
small, caducous. Synflorescences terminal or axillary; cyathia
zygomorphic, cyathophylls red to green, spreading or not, variously shaped, glands 2–6, appendiculate, situated on dorsal
side of involucre and usually enclosed in a spur-like extension
of the involucre tube; seeds ecarunculate.
Distribution and habitat. – Mexico, Central America, West
Indies, northern South America, southeastern U.S.A. (Florida);
desert scrub, as well as dry and wet tropical forests, sea level
to ca. 800 m.
Species included (15). – E. bracteata Jacq., E. calcarata
(Schltdl.) V.W. Steinm., E. coalcomanensis (Croizat) V.W.
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Steinm., E. colligata V.W. Steinm., E. conzattii V.W. Steinm.,
E. cymbifera (Schltdl.) V.W. Steinm., E. cyri V.W. Steinm.,
E. diazlunana (J. Lomelí & Sahagun) V.W. Steinm., E. dressleri
V.W. Steinm., E. finkii (Boiss.) V.W. Steinm., E. lomelii
V.W. Steinm., E. peritropoides (Millsp.) V.W. Steinm., E. personata (Croizat) V.W. Steinm., E. tehuacana (Brandegee)
V.W. Steinm., E. tithymaloides L.
Euphorbia sect. Crepidaria corresponds to the former
genus Pedilanthus and is a collection of fifteen species from
a wide range of habitats. The highly modified, zygomorphic
cyathia in which a nectar spur is constructed of both involucre and gland appendage tissue easily distinguish this group
(Dressler, 1957).
11. Euphorbia sect. Stachydium Boiss. in Candolle, Prodr.
15(2): 9, 65. 1862 – Type (see Wheeler in Amer. Midl.
Naturalist 30: 481. 1943): Euphorbia comosa Vell.
Monoecious herbs or shrubs; stems green, terete, laxly to
densely branched. Leaves ovate to linear-lanceolate, petiolate
or sessile, drought deciduous (except E. comosa); synflorescenses monochasial spikes; cyathia sessile, solitary, subtended
by a foliaceous bract, which overlaps with those of the other
cyathia, glands 4(5), elliptic, green-yellow, appendages lacking. Capsules elongate, glabrous, pedicillate, recurved or erect;
seeds tetragonous, tuberculate, carunculate.
Distribution and habitat. – Northern South America to
eastern Brazil; low deciduous forest and thorn scrub on sandy
or loose stony soils or rocky outcrops; 200–1200 m.
Species included (6). – E. comosa Vell., E. gollmeriana
Klotzsch ex Boiss., E. heterodoxa Mull.-Arg., E. invaginata
Croizat, E. lagunillarum Croizat, E. vervoorstii Subils.
12. Euphorbia sect. Brasilienses V.W. Steinm. & Dorsey, sect.
nov. – Type: Euphorbia phosphorea Mart.
Monoecious, xerophytic, stem-succulent shrubs to 6 m tall,
highly branched. Stems ascending, with a persistent green epidermis, 4–6 angles descending from leaf scars, waxy. Leaves
alternate, highly reduced and quickly deciduous, ovate, apex
acute, margin entire, secondary venation not evident. Cyathia
axillary, solitary or few in dense clusters, subsessile, glands
4–5(–7), transversely oblong, slightly cup-shaped with two
horns either spreading or ascending, red or yellow, situated on
the rim of the involucre; gynophore terminating in 3 triangular
calyx-like lobes; ovary glabrous, styles united most of their
length into a slender column, undivided. Capsule exserted from
the involucre, green, red, or yellow and red, glabrous, 3-lobed;
seeds obloid, rounded to weakly quadrangular in cross-section,
base and apex rounded, smooth to minutely papillate, with a
minute discoid caruncle.
Distribution and habitat. – Brazil (Espírito Santo, Bahia,
Minas Gerais, Paraíba, Pernambuco); rocky uplands (campos
rupestres), grasslands, thorn scrub, and tropical deciduous forest; 300–1250 m.
Species included (4). – E. attastoma Rizzini, E. holochlorina Rizzini, E. phosphorea Mart., E. sipolisii N.E. Br.
This is the only New World section comprised entirely
of stem-succulent species. The group is easily recognized by
Version of Record (identical to print version).
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
this habit and the colorful (dark red or yellow), horned cyathial
glands (Fig. 1K). The distinctions among species are mainly of
gland color and number of stem angles (Rizzini, 1987; Eggli,
1994).
13. Euphorbia sect. Pachysanthae X. Aubriot & Haev., sect.
nov. – Type: Euphorbia pachysantha Baill.
Shrubs to large trees (2–25 m), “bottle-shaped” and unbranched at the base, mostly monoecious. Stems succulent toward the apices; bark gray, smooth to wrinkled. Leaves spirally
arranged, grouped at the apices of the branches, obovate to
lanceolate, thick (except in E. pachysantha); stipules reduced
to two small glands. Synflorescence subterminal, 1 or 2–4
cyathia at the apex of the twigs; cyathophylls 2, well-developed,
green-yellow, soon deciduous; glands 5, stipitate, elliptic to
reniform, exappendiculate, green-yellow. Capsule indehiscent
or tardily dehiscent (dehiscence line present though dehiscence
not observed), erect or pendant, 3-locular or more commonly
2-locular or 1-locular by abortion, smooth to slightly wrinkled,
green when young, 1.5–4 cm diam.; seeds 1–3, smooth, globular, ecarunculate.
Distribution and habitat. – Madagascar; in a variety of
habitats, such as thickets in xeric bush of the southeast, tsingy
(karst) formations in the north, remnant forests in the high plateaus in the northwest, and rainforest relicts of the central east.
Species included (4). – E. mananarensis Leandri, E. mandravioky Baill., E. pachysantha Baill., E. pirahazo Jum.
The large, uni- or bilocular fruits of this section are quite
rare in Euphorbia and their presence suggests a close relationship to E. sect. Pervilleanae. Although rarely collected, the
fruits of E. pachysantha are apparently fleshy and indehiscent.
There are two additional species from northern Madagascar
awaiting publication by Aubriot & al. (in prep.)
14. Euphorbia sect. Pervilleanae Haev. & X. Aubriot, sect.
nov. – Type: Euphorbia pervilleana Baill.
Usually dioecious shrubs to trees, non-succulent but with a
water-storing rootstock; bark smooth to exfoliating. Leaves alternate to subopposite, shape variable (linear, lanceolate, elliptic
to obovate, scale-like for E. intisy); stipules reduced to black
gland-like dots. Synflorescences terminal, male synflorescences
bearing a larger number of cyathia; cyathophylls green, inconspicuous, similar to dichasial bracts; glands 4–6, elliptic to bilabiate. Capsule functionally 2(3)-locular, dehiscent or indehiscent,
erect, smooth to pubescent, usually bearing ornaments such as
wings, spines, or tubercles; seeds (1)2(3), large (5–10 mm diam.),
chestnut-shaped, smooth or tuberculate, ecarunculate.
Distribution and habitat. – Widespread across Madagascar.
Species included (7). – E. adenopoda Baill., E. analamerae
Leandri, E. intisy Drake, E. pervilleana Baill., E. randrianjohanyi Haev. & Labat, E. rauhii Haev. & Labat, E. tetraptera
Baker.
This group was formerly included in E. sect. Denisophorbia, to which it is not closely related. The leafless E. intisy was
previously included in E. subg. Tirucalli but was shown to be
misplaced there (Haevermans, 2003), and this is confirmed
here (Fig. 2B).
15. Euphorbia sect. Tirucalli Boiss. in Candolle, Prodr. 15(2):
10, 94. 1862 ≡ Euphorbia subsect. Tirucalli (Boiss.) Benth.
& Hook. f., Gen. Pl. 3(1): 260. 1880 ≡ Euphorbia subg.
Tirucalli (Boiss.) S. Carter in Kew Bull. 40: 823. 1985 ≡
Arthrothamnus Klotzsch & Garke in Monatsber. Königl.
Preuss. Akad. Wiss. Berlin 1859: 251. 1860, non Rupr.
1848 ≡ Euphorbia sect. Arthrothamnus Boiss. in Candolle,
Prodr. 15(2): 10, 74. 1862 – Type: Euphorbia tirucalli L.
= Euphorbia sect. Armatocalli Croizat in Webbia 27: 180. 1972
– Type: Euphorbia stenoclada Baill.
Usually dioecious shrubs to trees. Stems more or less succulent, with alternate or subverticillate branching (dichotomous
in E. carunculifera), terete (some species have more or less
flattened apices, in E. stenoclada sterile twig apices turn into
spiny processes), bark much delayed, fissured, detaching in
plates (smooth), gray-brown. Leaves alternate, early caducous,
variable in size and shape depending on the species but never
well-developed; pubescence more or less developed (potentially
present on every part of the plant); stipules highly reduced, glandular or absent. Synflorescences subterminal (terminal), composed of one or more lateral dichasia, only the terminal cyathia
functional; male synflorescences with many more cyathia than
the female ones, cyathophylls green, inconspicuous, similar to
dichasial bracts; cyathia usually unisexual, glands 5, orbicular
to elliptic, convex or concave, green to red, more or less stipitate; female flower pedicellate, perianth remnants constituting
a 3-lobed calyx, styles 3, free to base or united partway down,
bifid, recurved. Capsule smooth and sometimes pubescent, pendent or erect, 3(4–6)-locular, green or red, orbicular to acutely
3(4–6)-angled, then more or less deeply lobed; seeds 3(4–6),
cylindrical to obtusely 4-angled, testa smooth, carunculate.
Distribution and habitat. – Widespread and most diverse
in Madagascar, also native in the Arabian Peninsula (Oman
and Yemen, including Socotra) and Africa (Angola, Namibia,
Somalia, South Africa). Euphorbia tirucalli is widespread
across Africa, but it is not clear where the species is native
(probably Madagascar and southern Africa). It is widely cultivated in India and in other tropical countries.
Species included (24). – E. alcicornis Baker, E. analalavensis Leandri, E. arahaka Poiss., E. arbuscula Balf. f., E. bariensis
S. Carter, E. boinensis Denis ex Humbert & Leandri, E. carunculifera L.C. Leach, E. congestiflora L.C. Leach, E. damarana L.C. Leach, E. decorsei Drake, E. enterophora Drake,
E. fiherenensis Poiss., E. gregaria Marloth, E. gummifera
Boiss., E. imerina Cremers, E. kamponii Rauh & Pétignat,
E. mainty (Poiss.) Denis ex Leandri, E. neochamaeclada
Bruyns, E. ramofraga Denis & Humbert ex Leandri, E. spissa
M. Thulin, E. stenoclada Baill., E. tirucalli L., E. uzmuk
S. Carter & J.R.I. Wood, E. xylophylloides Brongn. ex Lem.
16. Euphorbia sect. Rubellae Dorsey, sect. nov. – Type: Euphorbia rubella Pax.
Monoecious geophytes. Root a subglobose to cone-shaped
tuber or fibrous. Stems reduced and underground, tuberculate. Leaves elliptic in a rosette at ground level, long petiolate
(2–6 cm); stipules threadlike or absent. Synflorescences subapical, produced before leaves emerge or with them, peduncle
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
2–11 cm long, more or less branched; cyathophylls orbicularovate, fused dorsally in E. cryptocaulis; cyathia sessile, glands
4 + 2 due to one being divided, oblong-elliptic, red or yellow;
ovary exserted, oblong, smooth. Capsule long-exserted, oblong-ovoid; seeds ovoid, tuberculate, carunculate.
Distribution and habitat. – Northeastern Africa (Sudan,
Ethiopia, Kenya, Uganda); open sites in limestone crevices on
well-drained soil, or under bushes in evergreen or deciduous
bushland.
Species included (3). – E. brunellii Chiov., E. cryptocaulis
M.G. Gilbert, E. rubella Pax.
This group of geophtytes from northeast Africa is unique
in its cyathial gland morphology having 4 equal-sized glands
and 2 smaller ones produced by the division of a single gland
(Gilbert, 1987). Geophytes are present in several sections of
E. subg. Euphorbia, but this unusual gland structure makes this
restricted and small group easily recognizable. Bally (1967)
considered E. brunellii a variety of E. rubella, but Gilbert
(1995) treated them as separate species based on distinct root
morphology, leaf size, cyathophyll shape, and capsule shape.
We follow Gilbert (1995) and note that both the ndhF and ITS
sequences differ more between these two species than between
many other accepted species pairs in E. subg. Euphorbia.
17. Euphorbia sect. Goniostema Baill. ex Boiss. in Candolle,
Prodr. 15(2): 10, 77. 1862 – Type (Wheeler in Amer. Midl.
Naturalist 30: 485. 1943): Euphorbia lophogona Lam.
= Lacanthis Raf., Fl. Tellur. 2: 94. 1837 ≡ Euphorbia subg.
Lacanthis (Raf.) M.G. Gilbert in Kew Bull. 42: 238. 1987
≡ Euphorbia sect. Diacanthium Boiss. in Candolle, Prodr.
15(2): 10, 78. 1862 ≡ Sterigmanthe Klotzsch & Garcke in
Monatsber. Königl. Preuss. Akad. Wiss. Berlin 1859: 252.
1860 – Type: Lacanthis splendens (Bojer) Raf. (= Euphorbia milii Des Moul.).
= Euphorbia sect. Rhizanthopsis Croizat in Webbia 27: 178.
1972 – Type: Euphorbia francoisii Leandri.
Monoecious, prostrate geophytes, shrubs, or trees. Stems
more or less succulent, branching or not; bark smooth, gray.
Leaves alternate, persistent or deciduous; shape highly variable;
succulent in some taxa; petiole cylindrical or winged; stipular
structures from gland-like to spines, individual or gathered
in vertical comb-like structures, some branching, glabrous to
pubescent. Synflorescences lateral (subterminal), of a variable
number of cyathia (in some taxa, axillary buds can further
develop the inflorescence by producing new cyathia); cyathophylls 2 per cyathium, usually well-developed and usually
brightly colored, usually distinct from synflorescence bracts,
patent or tightly enclosing the cyathia; cyathia bisexual, protandrous or protogynous; glands (4)5(6), shape variable, spreading
or enveloping the involucre. Capsule dehiscent, smooth, erect,
3-locular; seeds 3, verrucose, ecarunculate.
Distribution and habitat. – Widespread across Madagascar;
in a wide variety of habitats from sea level to upper mountains.
Species included (77). – E. alfredii Rauh, E. ambarivatoensis Rauh & Bard.-Vauc., E. ambovombensis Rauh & Razaf.,
E. analavelonensis Rauh & Mangelsdorff, E. ankarensis
Boiteau, E. ankazobensis Rauh & Hofstätter, E. annamarieae
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TAXON 62 (2) • April 2013: 291–315
Rauh, E. aureoviridiflora (Rauh) Rauh, E. banae Rauh, E. beharensis Leandri, E. berevoensis Lawant & Buddens., E. berorohae Rauh & Hofstätter, E. beuginii Rebmann E. biaculeata
Denis, E. boissieri Baill., E. boiteaui Leandri, E. brachyphylla
Denis, E. bulbispina Rauh & Razaf., E. capmanambatoensis
Rauh, E. capuronii Ursch & Leandri, E. caput-aureum
Denis, E. cremersii Rauh & Razaf., E. croizatii Leandri,
E. cylindrifolia Marn.-Lap. & Rauh, E. decaryi Guillaumin,
E. delphinensis Ursch & Leandri, E. denisiana Guillaumin,
E. didiereoides Denis ex Leandri, E. duranii Ursch & Leandri,
E. erythrocucullata Mangelsdorff, E. fianarantsoae Ursch
& Leandri, E. francoisii Leandri, E. genoudiana Ursch
& Leandri, E. geroldii Rauh, E. gottlebei Rauh, E. guillauminiana Boiteau, E. hermanschwartzii Rauh, E. hexadenia
Denis, E. hofstaetteri Rauh, E. horombensis Ursch & Leandri,
E. iharanae Rauh, E. isalensis Leandri, E. itremensis Kimnach & Lavranos, E. kondoi Rauh & Razaf., E. labatii Rauh
& Bard.-Vauc., E. leuconeura Boiss., E. lophogona Lam.,
E. mahafalensis Denis, E. mainiana Poiss., E. mangelsdorffii Rauh, E. mangokyensis Denis, E. maromokotrensis
Rebmann, E. milii Des Moul., E. millotii Ursch & Leandri,
E. moratii Rauh, E. neobosseri (Rauh) Rauh, E. neohumbertii Boiteau, E. pachypodioides Boiteau, E. parvicyathophora
Rauh, E. paulianii Ursch & Leandri, E. pedilanthoides Denis,
E. perrieri Drake, E. primulifolia Baker, E. quartziticola
Leandri, E. razafindratsirae Lavranos, E. razafinjohanyi Ursch
& Leandri, E. retrospina Rauh & Gerold, E. robivelonae Rauh,
E. rossii Rauh & Buchloh, E. sakarahaensis Rauh, E. suzannae-marnierae Rauh & Pétignat, E. tardieuana Leandri,
E. thuarsiana Baill., E. tsimbazazae Leandri, E. tulearensis
(Rauh) Rauh, E. viguieri Denis, E. waringiae Rauh & Gérold.
Bruyns & al. (2006) circumscribed this section to include
the entire Old World clade II, but here we limit it to a more
restricted clade containing the type, E. lophogona¸ and other
species generally characterized by colorful cyathophylls. Section Goniostema is the largest clade in E. subg. Euphorbia on
Madagascar and occurs across the island in diverse habitats.
It is also a morphologically diverse clade including understory
trees and shrubs in moist habitats (e.g., E. geroldii), spiny xerophytic or succulent shrubs and dwarfs from more arid habitats
(E. milii complex), and geophytes in fire-prone regions and
unusual substrates (e.g., E. primulifolia, E. quartzicola).
18. Euphorbia sect. Deuterocalli Croizat in Webbia 27: 179.
1972 ≡ Euphorbia subsect. Deuterocalli (Croizat) Bruyns
in Taxon 55: 415. 2006 – Type: Euphorbia oncoclada Drake
(≡ Euphorbia alluaudii subsp. oncoclada (Drake) F. Friedmann & Cremers).
Dioecious shrubs or small trees. Stems succulent, terete
(sometimes jointed as in a string of sausages because of alternation between long shoot and brachyblast morphology), bark
gray, smooth, much delayed. Leaves alternate, soon deciduous,
reduced to scales or lanceolate and petiolate; stipules modified
as a waxy or glandular ring around the leaf insertion. Synflorescence lateral (subterminal), male cyathia usually more numerous; cyathophylls inconspicuous, green (identical to dichasial
bracts); cyathia pedunculate; glands 5, elliptical, green-yellow.
Version of Record (identical to print version).
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
Capsule dehiscent, erect, 3-locular, green, smooth, with ridges
tinted with purple; seeds 3, smooth, ecarunculate.
Distribution and habitat. – Widespread in Madagascar,
mostly in dry scrub or among rocks in moister habitats, sea
level to ca. 500 m.
Species included (3). – E. alluaudii Drake, E. cedrorum
Rauh & Hebding, E. famatamboay F. Friedmann & Cremers.
This is a well-supported clade containing three species of
trees that were previously grouped with E. tirucalli because
of their leafless, pencil-stem growth form and dioecy. However, they differ from E. sect. Tirucalli in their thicker, more
jointed stems, stipules that form glandular or waxy rings around
the leaf scars, and ecarunculate seeds. Euphorbia alluaudii
is treated here to include E. leucodendron Drake as well as
E. oncoclada Drake.
19. Euphorbia sect. Denisophorbia (Leandri) Croizat in
Webbia 27: 165. 1972 ≡ Euphorbia subsect. Denisophorbia
Leandri in Bull. Soc. Bot. France 104: 500. 1957 – Type:
Euphorbia pyrifolia Lam.
Monoecious or dioecious shrubs or trees, without spines,
sometimes with a basal caudex, the upper branching chandelierlike, with plagiotropic branches composed of one or more series
of hypopodia (long, leafless internodes) and apical brachyblasts
(very short branches with a rosette of leaves), the stems succulent
or not, bark smooth, green or reddish-brown. Leaves spirally
arranged, shape variable, present only at nodes or extremities of
branches, deciduous to persistent, membranaceous to coriaceous
(sometimes slightly succulent), petiolate or subsessile; stipules reduced to glandular dots. Synflorescences subterminal on brachyblasts, bearing few to many cyathia; cyathophylls 2, scarious and
inconspicuous to well-developed and showy, green to yellow;
glands (4)5(6), oval to kidney-shaped, green-yellow or pink.
Capsule dehiscent, 3-locular, erect, smooth, round or strongly
3-angled in cross-section; seeds smooth, spherical, ecarunculate.
Distribution and habitat. – Madagascar, Mayotte and
Comoro Islands, Seychelles, Mauritius.
Species included (14). – E. anakaranae Leandri, E. aprica
Baill., E. betacea Baill., E. boivinii Boiss., E. bongolavensis
Rauh, E. elliotii Leandri, E. hedyotoides N.E. Br., E. mahabobokensis Rauh, E. mangorensis Leandri, E. martinae Rauh,
E. physoclada Boiss., E. pyrifolia Lam., E. rangovalensis
Leandri, E. zakamenae Leandri.
This section is treated here in a more limited sense than
Leandri’s original circumscription of E. subsect. Denisophorbia. It includes a group of mostly dioecious species from Madagascar and other Indian Ocean islands that have a Terminaliatype of sympodial branching, with long arching branches
ending in short brachyblasts that bear the leaves and cyathia.
The group is currently under revision, and there appear to be
at least five new species awaiting description (Haevermans
& al., in prep.).
20. Euphorbia sect. Monadenium (Pax) Bruyns in Taxon 55:
411. 2006 ≡ Monadenium Pax in Bot. Jahrb. Syst. 19: 126.
1894 – Type: Monadenium coccineum Pax. (≡ Euphorbia
neococcinea Bruyns).
= Synadenium Boiss. in Candolle, Prodr. 15(2): 187. 1862 – Type:
Synadenium arborescens Boiss. (≡ Euphorbia cupularis
Boiss.).
= Stenadenium Pax in Bot. Jahrb. Syst. 30: 343. 1901 – Type:
Stenadenium spinescens Pax (≡ Euphorbia spinescens
(Pax) Bruyns).
= Endadenium L.C. Leach in Garcia de Orta, Sér. Bot. 1: 31.
1973 – Type: Endadenium gossweileri (N.E. Br.) L.C.
Leach (≡ Monadenium gossweileri N.E. Br. ≡ Euphorbia
neogossweileri Bruyns).
Monoecious geophytes, herbs, shrubs, or trees. Stems
terete to angled, ± fleshy to succulent. Leaves fleshy, stipules
apparently absent or modified as spines or glands. Synflorescences axillary cymes to single cyathia; cyathophylls conspicuous, persistent, partly united along one edge then partly surrounding the involucre, or free; cyathia sessile; glands united
into a horseshoe or ring that surrounds 5 involucral lobes.
Capsule 3-lobed, dehiscent, exerted (through notch in gland
ring if present); seeds oblong, carunculate.
Distribution and habitat. – Eastern, central, and southeastern tropical Africa; in a variety of mostly arid habitats: thickets,
rock outcrops, and other open areas.
Species included (90). – E. bianoensis (Malaisse & Lecron)
Bruyns, E. bicompacta Bruyns, E. biselegans Bruyns,
E. bisellenbeckii Bruyns, E. bisglobosa Bruyns, E. bodenghieniae (Malaisse & Lecron) Bruyns, E. catenata Bruyns,
E. chevalieri Bruyns, E. clarae (Malaisse & Lecron) Bruyns,
E. crenata (N.E. Br.) Bruyns, E. cupricola (Malaisse & Lecron)
Bruyns, E. cupularis Boiss, E. descampsii (Pax) Bruyns,
E. dilunguensis (Malaisse & Lecron) Bruyns, E. discoidea
(P.R.O. Bally) Bruyns, E. echinulata (Stapf) Bruyns, E. filiformis (P.R.O. Bally) Bruyns, E. friesii (N.E. Br.) Bruyns,
E. fwambensis (N.E. Br.) Bruyns, E. gammaranoi G. Will.,
E. gladiata (P.R.O. Bally) Bruyns, E. guentheri (Pax) Bruyns,
E. hedigeriana (Malaisse & Lecron) Bruyns, E. herbacea (Pax)
Bruyns, E. heteropoda Pax, E. iancannellii Bruyns, E. invenusta (N.E. Br.) Bruyns, E. kimberleyana (G. Will.) Bruyns,
E. kirkii (N.E. Br.) Bruyns, E. kundelunguensis (Malaisse)
Bruyns, E. letestuana (Denis) Bruyns, E. letouzeyana (Malaisse)
Bruyns, E. lindenii (S. Carter) Bruyns, E. lugardiae (N.E. Br.)
Bruyns, E. mafingensis (Hargreaves) Bruyns, E. magnifica
(E.A. Bruce) Bruyns, E. major (Pax) Bruyns, E. mamfwensis
(Malaisse & Lecron) Bruyns, E. maryrichardsiae G. Will.,
E. neoangolensis Bruyns, E. neoarborescens Bruyns, E. neocapitata Bruyns, E. neococcinea Bruyns, E. neocrispa Bruyns,
E. neocymosa Bruyns, E. neogillettii Bruyns, E. neoglabrata
Bruyns, E. neoglaucescens Bruyns, E. neogoetzei Bruyns,
E. neogossweileri Bruyns, E. neogracilis Bruyns, E. neohalipedicola Bruyns, E. neokaessneri Bruyns, E. neomontana
Bruyns, E. neoparviflora Bruyns, E. neopedunculata Bruyns,
E. neoreflexa Bruyns, E. neorubella Bruyns, E. neorugosa
Bruyns, E. neospinescens Bruyns, E. neostolonifera Bruyns,
E. neovirgata Bruyns, E. orobanchoides (P.R.O. Bally) Bruyns,
E. pereskiifolia Houllet ex Baill., E. pseudohirsuta Bruyns,
E. pseudolaevis Bruyns, E. pseudomollis Bruyns, E. pseudonudicaulis Bruyns, E. pseudopetiolata Bruyns, E. pseudoracemosa (P.R.O. Bally) Bruyns, E. pseudosimplex Bruyns,
Version of Record (identical to print version).
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
E. pseudostellata Bruyns, E. pseudotrinervis Bruyns, E. pseudovolkensii Bruyns, E. pudibunda (P.R.O. Bally) Bruyns,
E. renneyi (S. Carter) Bruyns, E. rhizophora (P.R.O. Bally)
Bruyns, E. ritchiei (P.R.O. Bally) Bruyns, E. schaijesii (Malaisse)
Bruyns, E. schubei Pax, E. shebeliensis (M.G. Gilbert) Bruyns,
E. spectabilis (S. Carter) Bruyns, E. spinulosa (S. Carter)
Bruyns, E. succulenta (Schweickerdt) Bruyns, E. syncalycina Bruyns, E. syncameronii Bruyns, E. torrei (L.C. Leach)
Bruyns, E. triangolensis Bruyns, E. umbellata (Pax) Bruyns,
E. yattana (P.R.O. Bally) Bruyns.
Euphorbia sect. Monadenium corresponds to the formerly
recognized genera Monadenium, Synadenium, and Endadenium. These were previously segregated from Euphorbia based
on modifications of the cyathial glands—fused into a ring in
Endadenium and Synadenium, or into a horseshoe shape in
Monadenium. These modified gland structures continue to
be phylogenetically informative, as the former Synadenium
and Endadenium species group closely together within E. sect.
Monadenium. These species can also be distinguished by their
reduced caruncle relative to the distinctive one of most other
species in the section. Euphorbia sect. Monadenium is another
example of the lability of growth form evolution in E. subg.
Euphorbia, since it contains nearly every form present in the
subgenus. Many species also bear spine-like structures of various forms that support their close relationship to both E. sect.
Goniostema and E. sect. Euphorbia, although the homology
of the “spines” in these three sections is not yet established
(Fig. 1N–P).
21. Euphorbia sect. Euphorbia – Type: Euphorbia antiquorum L.
= Elaeophorbia Stapf in Johnston, Pl. Liberia 2: 646. 1906 –
Type: Elaeophorbia drupifera (Thonn.) Stapf (≡ Euphorbia
drupifera Thonn.).
= Euphorbia sect. Aculeatae Haw. in Philos. Mag. Ann. Chem.
1: 275. 1827 – Type: Euphorbia caerulescens Haw.
= Euphorbia sect. Cereis Webb & Berthelot, Hist. Nat. Iles
Canaries 2(3): 255. 1847 – Type: Euphorbia canariensis L.
= Euphorbia sect. Caulanthium Boiss. in Candolle, Prodr. 15(2):
10, 76. 1862 – Type: Euphorbia sessiliflora Roxb.
= Euphorbia sect. Tekeanae Croizat in Bull. Jard. Bot. État
Bruxelles 15: 119. 1938 – Type: Euphorbia teke Schweinf.
= Euphorbia sect. Ballyeuphorbia Croizat in Webbia 27:
181. 1972 – Type: Euphorbia decidua P.R.O. Bally
& L.C. Leach.
Monoecious geophytes, shrubs or trees. Stems succulent,
green, photosynthetic (some species forming bark in older
stems), winged, angled or tuberculate. Leaves alternate or
spiral, usually strongly reduced and caducous, but large and
persistent in some tree or shrub species; stipules apparently
modified as spines (rarely fused) and borne on a spine-shield
subtending or surrounding the leaf that can also bear a pair
of prickles. Synflorescences axillary, simple (compound), dichasia usually of three cyathia; cyathophylls inconspicuous;
peduncles usually short; cyathia bisexual; glands 5, entire,
typically elliptical, yellow to red; female flower pedicellate.
Capsule 3-locular, globose to deeply acutely lobed, in a few
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TAXON 62 (2) • April 2013: 291–315
species fleshy and indehiscent; seeds subglobose to ovoid,
smooth to minutely tuberculate, ecarunculate.
Distribution and habitat. – Widespread across most of
Africa, the Arabian Peninsula, and in southern Asia from
Pakistan to Malaysia, Indonesia and Papua New Guinea; in
a wide variety of habitats, but especially in arid landscapes,
open areas, dry forests, scrub, rock outcrops, with some species
occurring in moist forests.
Species included (343). – E. abdelkuri Balf. f., E. abyssinica J.F. Gmel., E. acervata S. Carter, E. actinoclada S. Carter,
E. adjurana P.R.O. Bally & S. Carter, E. aeruginosa Schweick., E. ambacensis N.E. Br., E. ambroseae L.C. Leach,
E. amicorum S. Carter, E. ammak Schweinf., E. ammophila
S. Carter & Dioli, E. amplophylla Pax, E. angularis Klotzsch,
E. angustiflora Pax, E. antiquorum L., E. asthenacantha
S. Carter, E. atrocarmesina L.C. Leach, E. atroflora S. Carter,
E. atrox F.K. Horw. ex S. Carter, E. avasmontana Dinter,
E. awashensis M.G. Gilbert, E. baga A. Chev., E. baioensis
S. Carter, E. baleensis M.G. Gilbert, E. ballyana Rauh, E. ballyi S. Carter, E. baradii S. Carter, E. barnardii A.C. White,
R.A. Dyer & B. Sloane, E. baylissii L.C. Leach, E. beillei
A. Chev., E. bertemariae Bisseret & Dioli, E. biharamulensis
S. Carter, E. bitataensis M.G. Gilbert, E. borenensis M.G. Gilbert, E. bougheyi L.C. Leach, E. breviarticulata Pax, E. brevis N.E. Br., E. brevitorta P.R.O. Bally, E. burgeri M.G. Gilbert, E. buruana Pax, E. bussei Pax, E. bwambensis S. Carter,
E. cactus Ehrenb. ex Boiss., E. caducifolia Haines, E. caerulescens Haw., E. caloderma S. Carter, E. canariensis L.,
E. candelabrum Trémaux ex Kotschy, E. cannellii L.C. Leach,
E. carteriana P.R.O. Bally, E. cataractarum S. Carter, E. cattimandoo Elliot ex Wight, E. classenii P.R.O. Bally & S. Carter,
E. clavigera N.E. Br., E. clivicola R.A. Dyer, E. coerulans
Pax, E. collenetteae D. Al-Zahrani & El-Karemy, E. colubrina
P.R.O. Bally & S. Carter, E. columnaris P.R.O. Bally, E. complanata Warb., E. complexa R.A. Dyer, E. confinalis
R.A. Dyer, E. conspicua N.E. Br., E. contorta L.C. Leach,
E. cooperi N.E. Br. ex A. Berger, E. corniculata R.A. Dyer,
E. cryptospinosa P.R.O. Bally, E. cuneneana L.C. Leach,
E. cuprispina S. Carter, E. cupularis Boiss., E. curvirama
R.A. Dyer, E. cussonioides P.R.O. Bally, E. dalettiensis
M.G. Gilbert, E. darbandensis N.E. Br., E. dasyacantha
S. Carter, E. dauana S. Carter, E. dawei N.E. Br., E. debilispina L.C. Leach, E. decidua P.R.O. Bally & L.C. Leach,
E. decliviticola L.C. Leach, E. dedzana L.C. Leach, E. deightonii Croizat, E. dekindtii Pax, E. demissa L.C. Leach, E. densispina S. Carter, E. desmondii Keay & Milne-Redh.,
E. dichroa S. Carter, E. discrepans S. Carter, E. dispersa
L.C. Leach, E. dissitispina L.C. Leach, E. distinctissima
L.C. Leach, E. drupifera Thonn., E. dumeticola P.R.O. Bally
& S. Carter, E. eduardoi L.C. Leach, E. eilensis S. Carter,
E. elegantissima P.R.O. Bally & S. Carter, E. ellenbeckii Pax,
E. enormis N.E. Br., E. epiphylloides Kurz, E. erigavensis
S. Carter, E. erlangeri Pax, E. evansii Pax, E. excelsa
A.C. White, R.A. Dyer & B. Sloane, E. exilispina S. Carter,
E. eyassiana P.R.O. Bally & S. Carter, E. fanshawei
L.C. Leach, E. fascicaulis S. Carter, E. faucicola L.C. Leach,
E. fissispina P.R.O. Bally & S. Carter, E. fluminis S. Carter,
Version of Record (identical to print version).
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
E. forolensis L.E. Newton, E. fortissima L.C. Leach, E. fractiflexa S. Carter & J.R.I. Wood, E. franckiana A. Berger,
E. frankii Lavranos, E. fruticosa Forssk., E. furcata N.E. Br.,
E. fusiformis Buch.-Ham. ex D. Don, E. galgalana S. Carter,
E. garuana N.E. Br., E. geldorensis S. Carter, E. gemmea
P.R.O. Bally & S. Carter, E. gillettii P.R.O. Bally & S. Carter,
E. glochidiata Pax, E. godana Buddens., Lawant & Lavranos,
E. gracilicaulis L.C. Leach, E. graciliramea Pax, E. grandialata R.A. Dyer, E. grandicornis Goebel ex N.E. Br., E. grandidens Haw., E. grandifolia Haw., E. graniticola L.C. Leach,
E. greenwayi P.R.O. Bally & S. Carter, E. greuteri N. Kilian,
Kürschner & P. Hein, E. griseola Pax, E. groenewaldii
R.A. Dyer, E. gymnocalycioides M.G. Gilbert & S. Carter,
E. halipedicola L.C. Leach, E. handiensis Burchard, E. heterochroma Pax, E. heterospina S. Carter, E. hiernii (Croizat)
Oudejans, E. holmesiae Lavranos, E. horwoodii S. Carter
& Lavranos, E. hottentota Marloth, E. hubertii Pax, E. imitata
N.E. Br., E. immersa P.R.O. Bally & S. Carter, E. imparispina
S. Carter, E. inaequispina N.E. Br., E. inarticulata Schweinf.,
E. inculta P.R.O. Bally, E. ingens E. Mey. ex Boiss., E. ingenticapsa L.C. Leach, E. inundaticola L.C. Leach, E. isacantha
Pax, E. johannis S. Carter, E. jubata L.C. Leach, E. kalisana
S. Carter, E. kamerunica Pax, E. kaokoensis (A.C. White,
R.A. Dyer, & B. Sloane) L.C. Leach, E. keithii R.A. Dyer,
E. khandallensis Blatt. & Hallb., E. knobelii Letty, E. knuthii
Pax, E. lacei Craib, E. lactea Haw., E. laikipiensis S. Carter,
E. ledienii A. Berger, E. lenewtonii S. Carter, E. leontopoda
S. Carter, E. letestui J. Raynal, E. limpopoana L.C. Leach ex
S. Carter, E. lividiflora L.C. Leach, E. longispina Chiov.,
E. louwii L.C. Leach, E. luapulana L.C. Leach, E. lukoseana
S. Carter, E. lydenburgensis Schweick. & Letty, E. madinahensis Fayed & D. Al-Zahrani, E. magnicapsula S. Carter,
E. makallensis S. Carter, E. malevola L.C. Leach, E. margaretae S. Carter, E. marrupana Bruyns, E. marsabitensis
S. Carter, E. mayuranathanii Croizat, E. meenae S. Carter,
E. memoralis R.A. Dyer, E. meridionalis P.R.O. Bally
& S. Carter, E. michaelii Thulin, E. micracantha Boiss.,
E. migiurtinorum Chiov., E. mitriformis P.R.O. Bally
& S. Carter, E. mlanjeana L.C. Leach, E. momccoyae Lavranos, E. monacantha Pax, E. monadenioides M.G. Gilbert,
E. mosaica P.R.O. Bally & S. Carter, E. multiclava P.R.O. Bally
& S. Carter, E. mwinilungensis L.C. Leach, E. myrioclada
S. Carter, E. namuliensis Bruyns, E. nana Royle, E. neriifolia L., E. nicholasii Oudejans, E. nigrispina N.E. Br.,
E. nigrispinoides M.G. Gilbert, E. nivulia Buch.-Ham.,
E. nubigena L.C. Leach, E. nyassae Pax, E. nyikae Pax ex
Engl., E. obconica Bojer ex N.E. Br., E. obovalifolia A. Rich.,
E. odontophora S. Carter, E. officinarum L., E. oligoclada
L.C. Leach, E. opuntioides Welw. ex Hiern, E. otjingandu
Swanepoel, E. otjipembana L.C. Leach, E. paganorum
A. Chev., E. parciramulosa Schweinf., E. parviceps
L.C. Leach, E. patentispina S. Carter, E. perangusta
R.A. Dyer, E. perarmata S. Carter, E. perplexa L.C. Leach,
E. persistentifolia L.C. Leach, E. pervittata S. Carter,
E. petraea S. Carter, E. petricola P.R.O. Bally & S. Carter,
E. phillipsiae N.E. Br., E. phillipsioides S. Carter, E. piceoides
Thulin, E. piscidermis M.G. Gilbert, E. platyrrhiza
L.C. Leach, E. plenispina S. Carter, E. poissonii Pax, E. polyacantha Boiss., E. ponderosa S. Carter, E. proballyana
L.C. Leach, E. prona S. Carter, E. pseudoburuana P.R.O.
Bally & S. Carter, E. pseudocactus A. Berger, E. pteroclada
L.C. Leach, E. qarad Deflers, E. quadrangularis Pax,
E. quadrialata Pax, E. quadrilatera L.C. Leach, E. quadrispina S. Carter, E. quinquecostata Volkens, E. ramipressa
Croizat, E. ramulosa L.C. Leach, E. reclinata P.R.O. Bally
& S. Carter, E. reptans P.R.O. Bally & S. Carter, E. resinifera
O. Berg, E. restricta R.A. Dyer, E. richardsiae L.C. Leach,
E. ridleyi Croizat, E. robecchii Pax, E. rowlandii R.A. Dyer,
E. royleana Boiss., E. rubrispinosa S. Carter, E. rubromarginata L.E. Newton, E. rugosiflora L.C. Leach, E. samburuensis P.R.O. Bally & S. Carter, E. santapaui A.N. Henry,
E. sapinii De Wild., E. saudiarabica Fayed & D. Al-Zahrani,
E. saxorum P.R.O. Bally & S. Carter, E. scarlatina S. Carter,
E. schinzii Pax, E. schizacantha Pax, E. schmitzii L.C. Leach,
E. scitula L.C. Leach, E. sebsebei M.G. Gilbert, E. seibanica
Lavranos & Gifri, E. sekukuniensis R.A. Dyer, E. semperflorens L.C. Leach, E. septentrionalis P.R.O. Bally & S. Carter,
E. sepulta P.R.O. Bally & S. Carter, E. serendipita L.E. Newton, E. seretii De Wild., E. sessiliflora Roxb., E. setispina
S. Carter, E. similiramea S. Carter, E. songweana S. Carter,
E. speciosa L.C. Leach, E. spiralis Balf. f., E. stapfii A. Berger,
E. stellata Willd., E. stenocaulis Bruyns, E. strangulata
N.E. Br., E. subsalsa Hiern, E. subscandens P.R.O. Bally
& S. Carter, E. sudanica A. Chev., E. sumati S. Carter,
E. susan-holmesiae Binojkumar & Gopalan, E. taifensis Fayed
& D. Al-Zahrani, E. tanaensis P.R.O. Bally & S. Carter,
E. taruensis S. Carter, E. teixeirae L.C. Leach, E. teke Schweinf. ex Pax, E. tenuirama Schweinf. ex A. Berger, E. tenuispinosa Gilli, E. tescorum S. Carter, E. tetracantha Rendle,
E. tetracanthoides Pax, E. tetragona Haw., E. tholicola
L.C. Leach, E. tisserantii A. Chev. & Sillans, E. torta Pax
& K. Hoffm., E. tortilis Rottler ex Ainslie, E. tortirama
R.A. Dyer, E. tortistyla N.E. Br., E. triaculeata Forssk., E. triangularis Desf. ex A. Berger, E. trigona Mill., E. turbiniformis Chiov., E. turkanensis S. Carter, E. uhligiana Pax,
E. umbonata S. Carter, E. umfoloziensis Peckover, E. undulatifolia Janse, E. unicornis R.A. Dyer, E. unispina N.E. Br.,
E. vajravelui Binojk. & N.P. Balakr., E. vallaris L.C. Leach,
E. vandermerwei R.A. Dyer, E. venenata Marloth, E. venenifica Tremaux ex Kotschy, E. venteri L.C. Leach ex R.H. Archer
& S. Carter, E. viduiflora L.C. Leach, E. virosa Willd., E. vittata S. Carter, E. volkmanniae Dinter, E. vulcanorum S. Carter,
E. wakefieldii N.E. Br., E. waterbergensis R.A. Dyer, E. whellanii L.C. Leach, E. williamsonii L.C. Leach, E. xylacantha
Pax, E. zoutpansbergensis R.A. Dyer.
Euphorbia sect. Euphorbia is the largest and one of the
most distinctive groups in E. subg. Euphorbia. The defining
character for this clade is the spine-shield—a horny pad of
tissue subtending or surrounding each leaf base that typically
bears two or four spiny outgrowths. These outgrowths are
usually interpreted as a pair of stipular spines and a pair of
prickles (Carter, 1994). The vast majority of species in E. sect.
Euphorbia have spine-shields, but in a few species they have
been lost (e.g., E. piscidermis and geophytes like E. meenae).
Version of Record (identical to print version).
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Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
ACKNOWLEDGEMENTS
The authors would like to thank R. Becker, A. Moller, The National Museums of Kenya, G. Mwachala, E. Wabuyele, C. Maina,
R. Gereau, W. Kindeketa, F. Ismail, H. Suleiman, F. Mbago, N. Mollel
and the Missouri Botanical Garden for facilitating field work. We
thank R. Becker, A. Moller, A. Mass, P. Forster, R. Graveson,
P. Carrillo-Reyes, J.W. Horn, B.W. van Ee, K.J. Wurdack, Y. Yang,
R. van Veldhuisen and J. Keizer (International Euphorbia Society),
E. Sandoval (UC-Davis Botanical Conservatory), D. Hannon (Huntington Botanical Gardens), E. van Jaarsveld (Kirstenbosch Botanical
Garden), T. Dold, and especially R. Webb and T. Yocum at the Arid
Lands Greenhouses, Tucson, Arizona for generously providing plant
material. We are grateful to the curators and staff at BRI, DSM, EA,
G, GRA, K, MA, MEL, MICH, MO, NBG, NHT, P, and PRE for allowing us to examine or sample from their collections. We also thank
S. Pereira, H. Draheim, B.S. Wagner, and B. Oyserman for help with
lab work and J. Peirson and Y. Yang for invaluable advice and help
with revising the manuscript. This work was funded by the National
Science Foundation through a Planetary Biodiversity Inventory Grant
(DEB-0616533) and National Geographic Society award # 8568-08 to
PEB, a Winifred B. Chase Fellowship from the UM Matthaei Botanical Garden, a Rackham Graduate School Research Grant, and a UM
EEB Block Grant to BLD.
LITERATURE CITED
Aubriot, X. 2012. Radiations évolutives, “innovations clés” et notions
d’espèces dans le genre Euphorbia L. à Madagascar. Ph.D. Dissertation, Muséum National d’Histoire Naturelle, Paris, France.
Bally, P.R.O. 1967. Miscellaneous notes on the flora of Tropical East
Africa including description of new taxa, 35–37. Candollea 22:
255–263.
Barres, L., Vilatersana, R., Molero, J., Susanna, A. & GalbanyCasals, M. 2011. Molecular phylogeny of Euphorbia subg. Esula
sect. Aphyllis (Euphorbiaceae) inferred from nrDNA and cpDNA
markers with biogeographic insights. Taxon 60: 705–720.
Bernal, R., Mora, F. & Murillo, J. 2006. Euphorbia sinclairiana,
an older name for the widespread Euphorbia elata. Caldasia 28:
217–220.
Boissier, E. 1862. Euphorbieae. Pp. 3–188 in: Candolle, A.P. de (ed.),
Prodromus systematis naturalis regni vegetabilis, vol. 15(2). Paris:
Victor Mason and Fils.
Bridges, E.L. & Orzell, S.L. 2002. Euphorbia (Euphorbiaceae) section Tithymalus subsection Inundatae in the southeastern United
States. Lundellia 5: 59–78.
Bruyns, P.V., Mapaya, R.J. & Hedderson, T. 2006. A new subgeneric
classification for Euphorbia (Euphorbiaceae) in southern Africa
based on ITS and psbA-trnH sequence data. Taxon 55: 397–420.
http://dx.doi.org/10.2307/25065587
Bruyns, P.V., Klak, C. & Hanacek, P. 2011. Age and diversity in Old
World succulent species of Euphorbia (Euphorbiaceae). Taxon
60: 1717–1733.
Cacho, N.I., Berry, P.E., Olson, M.E., Steinmann, V.W. & Baum,
D.A. 2010. Are spurred cyathia a key innovation? Molecular systematics and trait evolution in the slipper spurges (Pedilanthus
clade: Euphorbia, Euphorbiaceae). Amer. J. Bot. 97: 493–510.
http://dx.doi.org/10.3732/ajb.0900090
Carter, S. 1994. A preliminary classification of Euphorbia subgenus
Euphorbia. Ann. Missouri Bot. Gard. 81: 368–379.
http://dx.doi.org/10.2307/2992103
314
TAXON 62 (2) • April 2013: 291–315
Dressler, R.L. 1957. The genus Pedilanthus. Contr. Gray Herb. 182:
1–188.
Edgar, R.C. 2004. MUSCLE: Multiple sequence alignment with high
accuracy and high throughput. Nucl. Acids Res. 32: 1792–1797.
http://dx.doi.org/10.1093/nar/gkh340
Edwards, E.J. & Donoghue, M.J. 2006. Pereskia and the origin of the
cactus life-form. Amer. Naturalist 167: 777–793.
http://dx.doi.org/10.1086/504605
Eggli, U. 1994. Xerophytic euphorbias from Brazil. Euphorbia J. 9:
11–23.
Forster, P.I. 1994. Revision of Euphorbia plumerioides Tejsm. ex
Hassk. (Euphorbiaceae) and allies. Austrobaileya 4: 245–264.
Gilbert, M.G. 1987. Two new geophytic species of Euphorbia with
comments on the subgeneric groupings of its African members.
Kew Bull. 42: 231–244. http://dx.doi.org/10.2307/4109908
Gilbert, M.G. 1995. Euphorbiaceae. Pp. 265–380 in: Edwards, S.,
Mesfin Tadesse & Hedberg, I. (eds.), Flora of Ethiopia and Eritrea.
Uppsala: Uppsala University; Addis Ababa: Addis Ababa University.
Haevermans, T. 2003. Le genre Euphorbia à Madagascar: Phylogénie
moléculaire et systématique. Ph.D. Dissertation, Muséum National
d’Histoire Naturelle, Paris, France.
Haevermans, T. & Labat, J.-N.l. 2004. A synoptic revision of the
Malagasy endemic Euphorbia pervilleana group. Syst. Bot. 29:
118–124. http://dx.doi.org/10.1600/036364404772974266
Haevermans, T., Hoffmann, P., Lowry, P.P., Labat, J.N. &
Randrianjohany, E. 2004. Phylogenetic analysis of the Madagascan Euphorbia subgenus Lacanthis based on ITS sequence
data. Ann. Missouri Bot. Gard. 91: 247–259.
Hall, T.A. 1999. BioEdit: A user-friendly biological sequence alignment
editor and analysis program for Windows 95/98/NT. Nucl. Acids.
Symp. Ser. 41: 95–98.
Hassall, D.C. 1977. The genus Euphorbia in Australia. Austral. J. Bot.
25: 429–453. http://dx.doi.org/10.1071/BT9770429
Horn, J.W., Van Ee, B.W. & Wurdack, K.J. 2011. The giant genus
Euphorbia (Euphorbiaceae): Deep phylogenetics and major evolutionary patterns. Symposium talk, International Botanical Conference, Melbourne, Australia.
Horn, J.W., Van Ee, B.W., Morawetz, J.J., Riina, R., Steinmann,
V.W., Berry, P.E. & Wurdack, K.J. 2012. Phylogenetics and
the evolution of major structural characters in the giant genus
Euphorbia L. (Euphorbiaceae). Molec. Phylogen. Evol. 63: 305–
326. http://dx.doi.org/10.1016/j.ympev.2011.12.022
Huelsenbeck, J.P. & Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
http://dx.doi.org/10.1093/bioinformatics/17.8.754
Lemmon, A.R.J.M.B., Stanger-Hall, K. & Lemmon, E.M. 2009.
The effect of missing data on phylogenetic estimates obtained
by maximum-likelihood and Bayesian inference. Syst. Biol. 58:
130–145. http://dx.doi.org/10.1093/sysbio/syp017
Marshall, D.C. 2010. Cryptic failure of partitioned Bayesian phylogenetic analyses: Lost in the land of long trees. Syst. Biol. 59: 108–117.
http://dx.doi.org/10.1093/sysbio/syp080
Marshall, D.C., Simon, C. & Buckley, T.R. 2006. Accurate branch
length estimation in partitioned Bayesian analyses requires accommodation of among-partition rate variation and attention to branch
length priors. Syst. Biol. 55: 993–1003.
http://dx.doi.org/10.1080/10635150601087641
Müller, K. 2005. The efficiency of different search strategies in estimating parsimony jackknife, bootstrap, and Bremer support. B. M. C
Evol. Biol. 5: 58. http://dx.doi.org/10.1186/1471-2148-5-58
Müller, K. 2006. Incorporating information from length-mutational
events into phylogenetic analysis. Molec. Phylogen. Evol. 38:
667–676. http://dx.doi.org/10.1016/j.ympev.2005.07.011
Nobel, P.S. 1988. Environmental biology of agaves and cacti. Cambridge: Cambridge University Press.
Olmstead, R.G. & Sweere, J.A. 1994. Combining data in phylogenetic
Version of Record (identical to print version).
TAXON 62 (2) • April 2013: 291–315
Dorsey & al. • Phylogenetics of Euphorbia subg. Euphorbia
systematics: An empirical approach using three molecular data sets
in the Solanaceae. Syst. Biol. 43: 467–481.
http://dx.doi.org/10.1093/sysbio/43.4.467
Park, K.R. & Jansen, R.K. 2007. A phylogeny of Euphorbieae subtribe
Euphorbiinae (Euphorbiaceae) based on molecular data. J. Pl. Biol.
50: 644–649. http://dx.doi.org/10.1007/BF03030608
Posada, D. & Crandall, K.A. 1998. MODELTEST: Testing the model
of DNA substitution. Bioinformatics 14: 817–818.
http://dx.doi.org/10.1093/bioinformatics/14.9.817
Prenner, G. & Rudall, P.J. 2007. Comparative ontogeny of the cyathium in Euphorbia (Euphorbiaceae) and its allies: Exploring the
organ-flower-inflorescence boundary. Amer. J. Bot. 94: 1612–1629.
http://dx.doi.org/10.3732/ajb.94.10.1612
Rambaut, A. & Drummond, A. 2007. Tracer, version 1.5. Insitute of
Evolutionary Biology, University of Edinburgh. http://beast.bio
.ed.ac.uk/Tracer
Riina, R. & Berry, P.E. (coord.) 2012. Euphorbia planetary biodiversity
inventory database. http://app.tolkin.org/projects/72/taxa
Rizzini, C.T. 1987. Cactiform species of Euphorbia from Brazil
(Euphorbiaceae). Revista Brasil. Biol. 49: 979–997.
Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
http://dx.doi.org/10.1093/bioinformatics/btg180
Samuel, R., Kathriarachchi, H., Hoffmann, P., Barfuss, M.H.J.,
Wurdack, K.J., Davis, C.C. & Chase, M.W. 2005. Molecular
phylogenetics of Phyllanthaceae: Evidence from plastid matK and
nuclear phyC sequences. Amer. J. Bot. 92: 132–141.
http://dx.doi.org/10.3732/ajb.92.1.132
Shaw, J., Lickey, E.B., Beck, J.T., Farmer, S.B., Liu, W., Miller, J.,
Siripun, K.C., Winder, C.T., Schilling, E.E. & Small, R.L. 2005.
The tortoise and the hare II: Relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Amer. J. Bot. 92:
142–166. http://dx.doi.org/10.3732/ajb.92.1.142
Simmons, M.P. & Ochoterena, H. 2000. Gaps as characters in sequence-based phylogenetic analyses. Syst. Biol. 49: 369–381.
http://dx.doi.org/10.1093/sysbio/49.2.369
Staden, R. 1996. The Staden sequence analysis package. Molec. Biotechnol. 5: 233–241. http://dx.doi.org/10.1007/BF02900361
Stamatakis, A. 2006. RAxML-VI-HPC: Maximum likelihood-based
phylogenetic analyses with thousands of taxa and mixed models.
Bioinformatics 22: 2688–2690.
http://dx.doi.org/10.1093/bioinformatics/btl446
Steinmann, V.W. & Porter, J.M. 2002. Phylogenetic relationships in
Euphorbieae (Euphorbiaceae) based on ITS and ndhF sequence
data. Ann. Missouri Bot. Gard. 89: 453–490.
http://dx.doi.org/10.2307/3298591
Steinmann, V.W., Van Ee, B., Berry, P.E. & Gutierrez, J. 2007. The
systematic position of Cubanthus and other shrubby endemic species of Euphorbia (Euphorbiaceae) in Cuba. Anales Jard. Bot.
Madrid 64: 123–133.
Urbatsch, L.E., Baldwin, B.G. & Donoghue, M.J. 2000. Phylogeny
of the coneflowers and relatives (Heliantheae: Asteraceae) based
on nuclear rDNA internal transcribed spacer (ITS) sequences and
chloroplast DNA restriction site data. Syst. Bot. 25: 539–565.
http://dx.doi.org/10.2307/2666695
White, A.C., Dyer, R.A. & Sloan, B. 1941. The succulent Euphorbieae,
2 vols. Padasena: Abbey Gardens Press.
White, T.J., Bruns, T., Lee, S. & Taylor, J.W. 1990. Amplification
and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pp. 315–324 in: Innis, M.A., Gelfand, D.H., Sninsky,
J.J. & White, T.J. (eds.), PCR protocols: A guide to methods and
applications. San Diego: Academic Press.
Wilgenbusch, J.C., Warren, D.L. & Swofford, D.L. 2004. AWTY:
A system for graphical exploration of MCMC convergence in
Bayesian phylogenetic inference. School of Computation Sciences,
Florida State University. http://ceb.csit.fsu.edu/awty
Yang, Y., Riina, R., Morawetz, J.J., Haevermans, T., Aubriot, X.
& Berry, P.E. 2012. Molecular phylogenetics and classification
of Euphorbia subgenus Chamaesyce (Euphorbiaceae). Taxon 61:
764–789.
Zimmermann, N.F.A., Ritz, C.M. & Hellwig, F.H. 2010. Further
support for the phylogenetic relationships within Euphorbia L.
(Euphorbiaceae) from nrITS and trnL-trnF IGS sequence data.
Pl. Syst. Evol. 286: 39–58.
http://dx.doi.org/10.1007/s00606-010-0272-7
Version of Record (identical to print version).
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