Su & al. • Phylogenetic relationships of Santalales
TAXON 64 (3) • June 2015: 491–506
Phylogenetic relationships of Santalales with insights into the origins
of holoparasitic Balanophoraceae
Huei-Jiun Su,1 Jer-Ming Hu,1 Frank E. Anderson,2 Joshua P. Der3 & Daniel L. Nickrent4
1 Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei, 106, Taiwan
2 Department of Zoology, Southern Illinois University, Carbondale, Illinois 62901-6509, U.S.A.
3 Department of Biological Sciences, California State University Fullerton, Fullerton, California 92834-6850, U.S.A.
4 Department of Plant Biology, Southern Illinois University, Carbondale, Illinois 62901-6509, U.S.A.
Author for correspondence: Daniel L. Nickrent, nickrent@plant.siu.edu
ORCID: HJS, http://orcid.org/0000-0001-5751-7260; JMH, http://orcid.org/0000-0003-2739-9077; FEA, http://orcid.org/0000-0002
-5786-0314; JPD, http://orcid.org/0000-0001-9668-2525; DLN, http://orcid.org/0000-0001-8519-0517
DOI http://dx.doi.org/10.12705/643.2
Abstract To date molecular data have not revealed the exact phylogenetic position of Balanophoraceae in relation to hemiparasitic Santalales. To elucidate the phylogeny of Santalales and the position of Balanophoraceae, three plastid genes (matK,
rbcL, accD), three nuclear genes (SSU and LSU rDNA and RPB2) and one mitochondrial gene (matR) from 197 Santalales
samples (including 11 Balanophoraceae species) were analyzed with parsimony, maximum likelihood and Bayesian inference
methods. Our results demonstrate that Balanophoraceae is composed of two well-supported clades: a relatively slow-evolving
one including Dactylantus, Hachettea, and Mystropetalon (Mystropetalaceae) and an extremely fast-evolving one composed
of the remaining Balanophoraceae s.str. Support for monophyly of the two clades was low, thus it appears holoparasitism has
arisen twice independently in Santalales. These two clades appeared during a time of great change in the order (ca. 100 Ma)
when several major evolutionary innovations emerged, e.g., the root hemiparasites of Santalaceae s.l., the first aerial parasites
(Misodendraceae), herbaceous root parasites (Schoepfiaceae), root parasitic Loranthaceae (the ancestors of aerial parasitic
mistletoes), as well as the holoparasites in Balanophoraceae and Mystropetalaceae.
Keywords Balanophoraceae; molecular phylogeny; Mystropetalaceae; parasitic plant; Santalales
Supplementary Material Electronic Supplements 1 (Appendix S1; Figs. S1–S7) and 2 (Appendix 1 in tabular form) and
alignment are available in the Supplementary Data section of the online version of this article at http://www.ingentconnect
.com/content/iapt/tax
INTRODUCTION
The sandalwood order (Santalales) is worldwide in distribution and is the largest order of parasitic plants including
ca. 179 genera and 2460 species. Unlike most parasitic angiosperms, many members are woody and habits include both root
and stem parasites such as mistletoes. Placement of Santalales
within the global angiosperm phylogeny has previously been
uncertain despite strong support for monophyly of the clade
(Soltis & al., 1999, 2003; Hilu & al., 2003). More recent analyses
using chloroplast genes have shown that Santalales is strongly
supported as sister to a clade referred to as Superasteridae that
contains 12 other orders including Caryophyllales and Asterales
(Moore & al., 2010; Ruhfel & al., 2014). Features that unite
all Santalales includes simple leaves, valvate perianth, freecentral pendulous placentation (including reduced derivations),
and one-seeded fruits. Moreover, many members have C18
(and longer chain) acetylenic fatty acids such as santalbic acid
(Aitzetmüller, 2012; Kubitzki, 2015).
Reviews of the complex taxonomic history of Santalales
have been made (Reed, 1955; Kuijt, 1968, 2015; Malécot, 2002;
Nickrent & al., 2010). From the 19th century to present, there
has been a trend towards recognizing the mutual affinities
among a core group composed of seven families in a single
order, Santalales: Olacaceae, Misodendraceae, Loranthaceae,
Opiliaceae, Eremolepidaceae, Santalaceae and Viscaceae
(Kuijt, 1968; Cronquist, 1981). A number of other families, such
as Medusandraceae (Wurdack & Davis, 2009), Dipentodont
aceae (Peng & al., 2003), Grubbiaceae (Xiang & al., 2002)
have also been included at one time or another but the current
consensus is that they are not closely related.
The association of Balanophoraceae with Santalales dates
to the middle of the 19th century. Eichler (1867) provided
detailed descriptions and illustrations of female flowers among
various genera of Balanophoraceae and Cynomoriaceae. He
stated that Cynomoriaceae was allied with Hippuris L. (Saxifragales: Haloragaceae), in agreement with Hooker (1856) and
that Balanophoraceae (minus Mystropetalon Harv.) were related
Received: 18 Dec 2014 | returned for (first) revision: 18 Feb 2015 | (last) revision received: 8 Mar 2015 | accepted: 9 Mar 2015 || publication date(s):
online fast track, 27 May 2015; in print and online issues, 25 Jun 2015 || © International Association for Plant Taxonomy (IAPT) 2015
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to Misodendraceae and Loranthaceae. A connection to Santalales was maintained by Van Tieghem (1896), and Fagerlind
(1948), both of whom were influenced by shared morphological reductions in the gynoecium. Kuijt (1968, 1969) speculated
that these morphological similarities could be the results of
convergent adaptions to parasitism. Some 20th century classifications included these parasites in Santalales (Engler & Gilg,
1912; Cronquist, 1981) whereas some did not (Kuijt, 1968;
Takhtajan, 1997). In all of these more recent classifications,
Cynomoriaceae was included in Balanophoraceae or allied with
it. Takhtajan (1997) placed superorder Balanophoranae near
Rafflesianae, both in Magnoliidae. Balanophorales was split
into eight families that corresponded with the subfamilies and
tribes of Harms (1935). Later Takhtajan (2009) moved Balano
phoranae to Rosidae, placing it after Santalanae, and reunited
the segregate families into Balanophoraceae. These dramatically different taxonomic concepts, even among treatments
from the same individual, demonstrate well the uncertainty
about affinities of this group of holoparasites.
Clarification of relationships within and between Santalales
and Balanophoraceae began with the introduction of molecular
data. The first molecular phylogenetic study of Santalales that
included robust taxon sampling was by Nickrent & Duff (1996).
This study established the basic topological structure of the
phylogenetic tree with Olacaceae s.l. as basalmost followed by
Misodendraceae, Loranthaceae, Opiliaceae, Santalaceae and
Viscaceae. Schoepfia Schreb. was shown to be more closely
related to Misodendraceae and “Eremolepidaceae” a component of Santalaceae s.l. Small-subunit rDNA sequences were
used to generate this phylogeny and were also used to show a
split between the Old and New World genera of Balanophor
aceae. That study did not address any possible relationships
between Santalales and Balanophoraceae, mainly because of
high substitution rates in the holoparasites (Nickrent & Starr,
1994) that compromised via long-branch attraction (LBA) parsimony analyses with other angiosperms. Later work using both
nuclear ribosomal and mitochondrial gene sequences showed
that Cynomoriaceae was not closely related to Balanophoraceae and that the later was most closely related to Santalales
(Nickrent & al., 2005). Both of these relationships were later
confirmed in the large-scale study of parasite evolution by
Barkman & al. (2007). Further confirmation of a Santalales
affinity came from molecular phylogenies of nuclear RPB2
and B-class genes (Su & Hu, 2012). Despite these advances, the
exact placement of Balanophoraceae, either sister to or within
Santalales, was not resolved.
Relationships within Santalales (not including Balanophor
aceae) have been explored in several molecular phylogenetic
investigations: Olacaceae s.l. (Malécot & Nickrent, 2008),
Loranthaceae (Vidal-Russell & Nickrent, 2008a), and Santal
aceae s.l. (Der & Nickrent, 2008). The timing of the evolution
of the mistletoe habit was examined using 36 representatives of
Santalales (Vidal-Russell & Nickrent, 2008b). These data were
summarized and a new classification of the order proposed by
Nickrent & al. (2010). Although a consensus phylogeny was
presented, this did not derive from an alignment containing
all known sequences for the order.
492
In the present study, sequence data from the nucleus, chloroplast and mitochondrion have been assembled for all available Santalales including Balanophoraceae. For the first time,
analyses were conducted with a 7-gene matrix to examine (1)
support for all Santalales clades (families) and (2) the phylogenetic position of Balanophoraceae in the sandalwood order.
MATERIALS AND METHODS
Taxon sampling. — A total of 19 families, 148 genera and
180 species of Santalales were sampled, including 10 genera and
11 species of Balanophoraceae (Appendix 1, with voucher information and GenBank accession numbers). Six species from other
core eudicots were used as the outgroups. Although some classifications include Cynomorium L. within or near Balanophor
aceae (Cronquist, 1981; Takhtajan, 2009), it was not included in
this study (justification in Electr. Suppl.: Appendix S1).
DNA extraction and gene amplifications. — For the newly
obtained sequences in this study, genomic DNA was extracted
from herbarium, fresh frozen or silica dried plant tissues using
a standard CTAB method (Doyle & Doyle, 1987) or a modified CTAB method (Nickrent, 1994, 1997). Chloroplast matK
and accD genes were amplified using primers and protocols
reported in Rogers & al. (2008). Nuclear LSU rDNA genes were
amplified according to Vidal-Russell & Nickrent (2008a). The
nuclear SSU rDNA, mitochondrial matR and the homologs of
RPB2 sequences were amplified with the primers and conditions described in Su & Hu (2012). Direct sequencing of PCR
products used various automated methods. Additionally, five
sequences were extracted from four transcriptome assemblies
included in the 1000 Plants Project (1KP; http://www.onekp
.com) using BLAST, including Dendropemon caribaeus Krug
& Urb. (accD, RPB2), Phoradendron leucarpum (Raf.) Reveal
& M.C.Johnst. (RPB2), Exocarpos cupressiformis Labill.
(RPB2), and Daenikera corallina Hürl. & Stauffer (RPB2).
Phylogenetic analyses. — Edited sequences were imported
into Se-Al v.2.0a11 (Rambaut, 2007) and aligned manually. For
the protein coding genes, the nucleotide sequences were translated into amino acid sequences and indels were introduced
while maintaining sequence frame. All indels were treated as
missing data. For nuclear ribosomal DNA, alignment was guided
by reference to published higher-order structures. Individual
gene alignments were saved as NEXUS files and then concatenated using Mesquite v.3.01 (Maddison & Maddison, 2011).
All of the individual gene datasets and the concatenated
datasets were analyzed using maximum parsimony (MP), maximum likelihood (ML) and Bayesian inference (BI) methods.
For the ML and BI analyses, appropriate substitution models for each individual gene dataset were estimated using
jModelTest v.2.1.3 (Posada, 2008, 2009). The ML topologies
were performed under Genetic Algorithm for Rapid Likelihood Inference (Garli) v.2.0 (Zwickl, 2006). 100 search replicates with stepwise addition of taxa and all other options set
to defaults. Rapid bootstrapping (BS) of 500 pseudo-replicates
was performed in RAxML v.7.0.4 (Stamatakis, 2006) under
the GTR + I + G model. The BI analyses were performed with
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MrBayes v.3.1.2 (Ronquist & Huelsenbeck, 2003) and the bestfitting substitution model for the combined datasets were estimated using PartitionFinder v.1.1.1 (Lanfear & al., 2012) for each
gene and codon position. Markov Chain Monte Carlo searches
were performed with four chains of 2.5 (individual gene datasets) or 7 (concatenated dataset) million generations with a
sample frequency of 500. The consensus tree and Bayesian
inference posterior probabilities (BIPP) were calculated from
trees with split frequencies less than 0.01.
For the MP analyses, heuristic searches were conducted
by PAUP* v.4.01b10 (Swofford, 2002) with 1000 random addition replicates using tree bisection-reconnection (TBR) branch
swapping with steepest descent option in effect. The maximum
trees were set to 10,000 and 1 tree was held at each step. The MP
bootstrap were evaluated using 100 random-addition replicates
with the maximum trees retained set to 10,000, retaining only
10 trees of length ≥ 1 per replicate (nchuck = 10, chuckscore = 1).
Hypothesis testing. — Multiple tests were conducted to
assess possible conflicts among different datasets and analytical approaches. Tree topologies and support values resulting
from each dataset were compared to assess the possible conflicts. To test the effects of different data and different inference
methods on the phylogenetic estimation, we performed the MP/
ML analyses with varying gene content: (1) removing the fastevolving taxa of Balanophoraceae in the 7-gene concatenated
dataset and (2) removing the third-codon position of proteincoding genes in the non-plastid gene dataset.
Trees resulting from MP and ML analyses of the concatenated dataset supported different hypotheses of relationships
among members of Balanophoraceae. Two simulation-based
tests were conducted to assess whether monophyly of Balano
phoraceae can be rejected under ML and if MP is being misled
by LBA. A parametric bootstrapping test called SOWH (Swofford & al., 1996) was implemented to evaluate the hypothesis
that a tree on which Balanophoraceae is monophyletic is the
best explanation of the concatenated 7-gene dataset. The complexities of this dataset—i.e., alignment gaps in many of the
genes, missing data for some genes for some taxa, and no plastid data for Balanophoraceae—complicated the simulations.
To test this hypothesis, we estimated the best-fitting model for
each gene in jModelTest as described above, ignoring models
that included a proportion of invariant sites parameter (this
parameter is not available in PAML; see below). The ML tree
for the 7-gene dataset, partitioned by gene, was estimated in
Garli under a topological constraint that enforced monophyly
for Balanophoraceae. Each individual gene dataset was opened
in PAUP*; the ML tree was loaded into PAUP* along with
each individual-gene dataset. Taxa missing for each gene were
deleted from the ML tree, producing a trimmed ML tree based
on the full dataset that matched the complement of taxa for
which data were available for each gene. Each of the seven
resulting trimmed trees was loaded into PAML v.4.3 (Yang,
2007) along with the corresponding individual gene dataset,
and branch lengths of the trimmed tree and substitution model
parameters were estimated for each gene. The seven sets of
trimmed tree topology, branch lengths and model parameter
estimates were individually used to simulate 100 single-gene
datasets in INDELible v.1.03 (Fletcher & Yang, 2009). These
100 simulated single-gene data matrices were concatenated
using FASconCAT v.1.0pl (Kück & Meusemann, 2010). The
resulting simulated 7-gene concatenated datasets did not
include indels within genes, but did match the original concatenated dataset’s pattern of missing data on a “by locus”
basis (i.e., taxa missing data for genes in the original data also
lacked these data in the simulated concatenated data matrices).
The simulated datasets were analyzed in Garli with and without
enforcing a topological constraint for Balanophoraceae monophyly. Garli analyses were conducted using five random stepwise addition search replicates, with data partitioned by gene
and using the best-fitting substitution models for each gene as
estimated for the original concatenated dataset. The resulting
delta values (differences in log likelihood for the pair of ML
trees estimated for each simulated dataset) were used as a null
distribution for the hypothesis that a tree including a monophyletic Balanophoraceae is the true tree. The observed delta value
(the difference in likelihood between the unconstrained ML
tree for the original dataset and the best ML tree found under a
Balanophoraceae monophyly constraint) was compared to this
null distribution. If the observed delta was greater than 95%
of the simulated delta values, the null hypothesis was rejected.
A similar test was used to investigate whether LBA could
be misleading MP, causing it to recover a monophyletic Balanophoraceae. Following (Huelsenbeck & Crandall, 1997), data
were simulated and concatenated as described above, but on the
unconstrained ML tree estimated by Garli via an analysis of the
original, 7-gene concatenated dataset with the data partitioned
by gene. These 100 simulated concatenated datasets were analyzed with MP as described above. Trees resulting from MP
analyses were passed through a Balanophoraceae monophyly
filter in PAUP*. If LBA is misleading MP, we expect MP to
return trees on which Balanophoraceae is monophyletic.
RESULTS
A total of 124 sequences were newly obtained in this study,
which including 7 SSU rDNA, 23 LSU rDNA, 39 RPB2, 1 rbcL,
3 matK, 34 accD and 17 matR gene sequences. Statistics relating to the separate and combined gene datasets and subsequent
phylogenetic analyses are given in Table 1. Among the seven
individual gene datasets, the plastid matK gene contained the
highest percentage of parsimony-informative characters (54%)
whereas the nuclear SSU rDNA exhibited the lowest (25%).
Although the level of resolution between the different datasets
differed, the relationships among the major clades were largely
congruent without a significant conflict (here we refer to BS >
60%) among the topologies (Electr. Suppl.: Fig. S1).
Phylogenetic analyses of combined datasets. — The
topologies of the 7-gene concatenated dataset from ML/BI
(Fig. 1, BI tree not shown) and MP (Electr. Suppl.: Fig. S2)
are all highly similar to each other. The monophyly of Santalales is well supported by all three methods (MP/ML BS
= 99%–100%, BIPP = 1.0) and the clades corresponding to
each of the Santalales families (except for Balanophoraceae)
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Table 1. Characteristics of different datasets.
Dataset
Taxa
Aligned
length (bp)
PI
sites
Tree
length
MP trees
CI
RI
ML model
accD
86
1,449
680
3,091
104,109
0.496
0.676
GTR + I + G
matK
166
1,929
1,042
7,035
4,070
0.358
0.758
GTR + I + G
rbcL
130
1,437
449
2,598
1,430
0.389
0.686
TVM + I + G
SSU rDNA
179
1,841
455
3,165
7,498
0.345
0.629
GTR + I + G
LSU rDNA
133
2,166
737
5,255
120
0.341
0.549
GTR + I + G
RPB2
54
1,716
682
4,934
8
0.284
0.424
GTR + I + G
matR
54
2,346
629
2,136
15,566
0.740
0.657
TIM + G
Plastid combined
172
4,815
2,171
12,840
530
0.394
0.727
TVM + I + G
Non-plastid combined
182
8,069
2,503
15,707
7,320
0.374
0.532
GTR + I + G
Non-plastid combined
(3rd codon removed)
182
6,715
1,725
10,562
30
0.395
0.575
GTR + I + G
7 genes combined
186
12,884
4,674
28,736
6,912
0.380
0.641
GTR + I + G & SYM + I + G
7 genes minus Bal. A
178
12,884
4,052
25,219
15,552
0.384
0.657
GTR + I + G
Abbreviations: PI, parsimony informative; MP, maximum parsimony; CI, consistency index; RI, retention index; ML, maximum likelihood; Bal.,
Balanophoraceae
A
Corynaea crassa
Helosis cayennensis
Lophophytum leandrii
Ombrophytum
Sarcophyte sanguinea
subterraneum
Thonningia sanguinea
73/.99/68
Dulacia candida
Olax emirnensis
Olax imbricata
Olax aphylla
Olax benthamiana
Ptychopetalum petiolatum
Coula edulis
Minquartia guianensis
Ochanostachys amentacea
Aptandra tubicina
Ongokea gore
Harmandia mekongensis
Hondurodendron urceolatum
Chaunochiton kappleri
Anacolosa papuana
Phanerodiscus capuronii
Cathedra acuminata
Curupira tefeensis
52/ - / Ximenia americana
Malania oleifera
Octoknema sp.
78/.98/80
Heisteria cauliflora
Heisteria parvifolia
52/.84/57
Heisteria concinna
Heisteria densifrons
Heisteria acuminata
Maburea trinervis
Erythropalum scandens
56/1.0/ Strombosiopsis tetrandra
-/-/Tetrastylidium peruvianum
Engomegoma gordonii
Diogoa zenkeri
Strombosia grandifolia
80/1.0/77
Strombosia philippinensis
Strombosia pustulata
Scorodocarpus borneensis
-/-/Antirrhinum majus
67/.99/ Cornus florida
- /1.0/81
Camellia japonica
Spinacia oleracea
Arabidopsis thaliana
Myrtus communis
79/.95/ 60/.52/ -
Balanophoraceae A
Balanophora laxiflora
Balanophora
fungosa
Olacaceae
Coulaceae
Aptandraceae
Ximeniaceae
Octoknemaceae
Erythropalaceae
Strombosiaceae
Outgroups
0.01 substitutions/site
Fig. 1A–C. The ML phylogram inferred from the 7-gene-combined dataset for Santalales. Bootstrap support greater than 80% and Bayesian
posterior probabilities greater than 0.95 are shown with bold lines. Lesser support values are given above the nodes: maximum likelihood bootstrap / Bayesian inference posterior probabilities / maximum parsimony bootstrap (MLBS/BIPP/MPBS). A, Bottom portion of the phylogram
showing relationships among Olacaceae s.l. and Balanophoraceae s.str. Two of the long branches in Balanophoraceae were split given graphical
constraints. B, Middle portion of the phylogram showing relationships among Misodendraceae, Schoepfiaceae, Balanophoraceae B (Mystro
petalaceae), and Loranthaceae. So as not to obscure the Loranthaceae clades, nodes were numbered (1–36) and the support values indicated next
to the tree. C, Upper portion of phylogram showing relationships among Opiliaceae and seven families sometimes classified as Santalaceae s.l.
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all received bootstrap support greater than 95%. However,
there are some topological differences between of ML/BI and
MP, including the relationships among Olacaceae, Coulaceae,
Aptandraceae, Octoknemaceae and Ximeniaceae, as well as the
relationships among Thesiaceae, Comandraceae, Cervantesi
aceae and Balanophoraceae. The position of Octoknemaceae
(consisting of one accession of Octoknema Pierre) was placed
at different positions on the trees (Fig. 1A; Electr. Suppl.: Fig.
S2), as one of the basal lineages in Santalales with ML/BI
(Fig. 1) or as sister to the “non-Olacaceae s.l.” taxa with MP
(Electr. Suppl.: Fig. S2). Some support for the latter position
was obtained with ML/BI using a dataset where the fast-evolving Balanophoraceae taxa were removed (Electr. Suppl.: Fig.
S3). The relationships among Olacaceae, Coulaceae, Aptandraceae and Ximeniaceae also varied between the ML/BI and MP
trees. Sister relationships were found between Olacaceae and
Aptandraceae and between Coulaceae and Ximeniaceae in the
MP analysis (Electr. Suppl.: Fig. S2) and the ML analysis without fast-evolving Balanophoraceae (ML/MP BS = 53%–78%,
BIPP = 0.95–1.0 in Electr. Suppl.: Fig. S3). However, in the ML
analysis with all Balanophoraceae, Coulaceae was resolved as a
sister to Olacaceae and the remaining “non-Olacaceae s.l. taxa;
moreover, Ximeniaceae was sister to Aptandraceae. In both of
these cases support for the clades was low.
In both the ML/BI and MP trees (Fig. 1A, B; Electr. Suppl.:
Fig. S7) Balanophoraceae are resolved as two well-supported
clades. The first, called Balanophoraceae A, is composed of
seven genera including Balanophora J.R.Forst. & G.Forst. and
the second, Balanophoraceae B, is composed of Dactylanthus
Hook.f., Hachettea Baill. and Mystropetalon. These two clades
have conspicuously different substitution rates resulting in the
former with very long intertaxon branch lengths whereas the
latter clade has branches comparable to other Santalales parasites (e.g., Viscaceae). The MP tree (Electr. Suppl.: Fig. S2)
B
80/.99/ -
1. 94/1.0/75
2. 55/.90/ 3. 84/1.0/75
4. - /.78/ 5. 70 /1.0/57
6. - /.80/ 7. 77/.99/67
8. 90/1.0/67
9. 57/.99/ 10. 50/.92/ 11. - /.55/ 12. - /.77/ 13. - /.76/ 14. 84/1.0/72
15. 81/1.0/ 16. 60/.73/67
17. 70/.89/ 18. 68/.92/83
19. 55/.91/ 20. - /.70/ 21. - /.78/ 22. 66/.87/ 23. 60/.79/59
24. 53/.57/ 25. 54/.75/ 26. 67/.57/73
27. 74/.57/72
28. -/.52/ 29. - / - / 30. 53/.99/ 31. 53/.77/ 32. 61/.76/62
33. -/.65/ 34. - /.75/ 35. - /.91/ 36. -/.96/74
80/.97/ -
100/.99/ -
100/1.0/54
Oncella ambigua
Oncocalyx sulfureus
Agelanthus sansibarensis
3
Actinanthella menyharthii
Englerina ramulosa
5
Tapinanthus constrictiflorus
4
Berhautia senegalensis
Oedina pendans
6
7
Emelianthe panganensis
Globimetula dinklagei
8
Erianthemum dregei
Oliverella rubroviridis
9
10
Moquiniella rubra
Phragmanthera crassicaulis
11
Bakerella sp.
Plicosepalus sagittifolius
12
Socratina bemarivensis
Vanwykia remota
13
Dendrophthoe curvata
15
Dendrophthoe longituba
14
Helixanthera coccinea
16
Scurrula parasitica
17
Scurrula pulverulenta
Scurrula ferruginea
Taxillus chinensis
18
Taxillus pseudochinensis
Helixanthera cylindrica
Amyema glabra
19
Diplatia furcata
20
Dactyliophora
novae-guineae
21
Amyema queenslandica
23
Benthamina alyxifolia
22
Sogerianthe sessiliflora
Baratranthus axanthus
Ileostylus micranthus
Muellerina eucalyptoides
Loranthus delavayi
Loranthus kaoi
Loranthus europaeus
Cecarria obtusifolia
Lepidaria forbesii
24
Macrosolen cochinchinensis
25
Decaisnina triflora
Amylotheca duthiana
Loxanthera speciosa
26
Lysiana filifolia
27
Lepeostegeres lancifolius
Alepis flavida
28
Peraxilla tetrapetala
Tupeia antarctica
29
30
Desmaria mutabilis
Struthanthus oerstedii
Struthanthus woodsonii
31
Cladocolea gracilis
Dendropemon bicolor
32
Oryctanthus occidentalis
Passovia pyrifolia
33
Aetanthus nodosus
34
Psittacanthus calyculatus
Tripodanthus acutifolius
35
Notanthera heterophylla
36
Ligaria cuneifolia
Tristerix corymbosus
Gaiadendron punctatum
Atkinsonia ligustrina
Nuytsia floribunda
Dactylanthus taylori
Hachettea austrocaledonica
Mystropetalon thomii
Schoepfia chinensis
Schoepfia jasminodora
Schoepfia schreberi
Arjona tuberosa
Quinchamalium chilense
Misodendrum linearifolium
Misodendrum punctulatum
1
2
Loranthaceae
Balanophoraceae B
Schoepfiaceae
Misodendraceae
0.01 substitutions/site
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shows Balanophoraceae as monophyletic but with low support
(MPBS < 50%). In contrast, Balanophoraceae are not monophyletic on the ML/BI tree (Fig. 1) with the B clade sister to
Loranthaceae (MLBS = 80%, BIPP = 0.97) and the A clade
sister to the “non-Olacaceae s.l.” clade (MLBS = 94%, BIPP =
1.0). After removal of the A clade in both the ML (Electr. Suppl.:
Fig. S3) and MP (Electr. Suppl.: Fig. S4) trees, the position of
the B clade remained the same, either sister to Loranthaceae
(MLBS = 93%, BIPP = 0.96) or grouped with Schoepfiaceae
and Misodendraceae (MPBS = 96%).
The large mistletoe family Loranthaceae received strong
support as monophyletic in all analyses with the root parasite
Nuytsia R.Br. sister to the rest of the family. Atkinsonia F.Muell.
also a root parasite from Australia, diverged next in both the
ML/BI (Fig. 1B) and MP (Electr. Suppl.: Fig. S2) trees. The
third root parasite, Gaiadendron G.Don. diverged next in the
ML/BI tree but not on the MP tree. The topology of these two
trees differed most in the positions of biogeographically key
taxa such as Tupeia Cham. & Schltdl. from New Zealand and
Desmaria Tiegh. and Notanthera G.Don. from South America.
In general, several clades from the “spine” of these trees were
poorly supported, thus resulting in low resolution.
The upper portion of the ML/BI (Fig. 1C) and MP (Electr.
Suppl.: Fig. S2) trees consisting of Opiliaceae and Santalaceae
s.l. were for the most part congruent. Opiliaceae (including
Anthobolus R.Br. of former Santalaceae) was resolved with
C
69/.95/73
strong support as sister to the remaining clades. The monophyly
of the other seven families received strong bootstrap support
with ML/BI and MP but interrelationships differed in some
cases. A sister relationship between Thesiaceae and Cervantesiaceae received moderate support (MLBS = 76%, BIPP = 0.78,
MPBS < 50%) and Comandraceae was sister to them (MLBS =
75%, BIPP = 0.65, MPBS < 50%). Despite showing these three
families in one clade on the shortest MP tree (Electr. Suppl.:
Fig. S2), support for this clade was low.
Comparing the topologies based on the plastid and nonplastid gene datasets. — The phylogenetic relationships of the
major clades based on ML and MP analyses of four non-plastid
and three plastid genes are shown in Fig. 2. The individual
genes contained different amounts of phylogenetic signal as
shown by the number of parsimony-informative sites (Table 1)
with the lowest being SSU rDNA and rbcL and the highest
matK and LSU rDNA. RPB2 and matR had the lowest taxon
sampling, which also influences comparisons of phylogenetic
signal across genes and partitions (Electr. Suppl.: Fig. S1).
Despite some incongruences between the ML and MP topologies in non-plastid and plastid data partitions, most of these
conflicted relationships received weak bootstrap support (MP/
ML BS < 60%).
Although support for clades representing the families
Olacaceae s.l. and Santalaceae s.l. were generally high, relationships between these clades (i.e., along the “spine” of the
Leptomeria aphylla
Leptomeria pauciflora
Spirogardnera rubescens
Choretrum pauciflorum
Dendromyza ledermannii
Dendrotrophe varians
Dufrenoya sphaerocarpa
Phacellaria rigidula
Amphorogyne celastroides
Daenikera corallina
85/.79/96
- /- / -/-/-
Phoradendron californicum
Phoradendron leucarpum
Dendrophthora clavata
Ginalloa arnottiana
Korthalsella lindsayi
Arceuthobium
Viscum album
verticilliflorum
Viscum articulatum
Notothixos subaureus
Santalum album
Santalum macgregorii
Antidaphne viscoidea
Myoschilos oblongum
Eubrachion ambiguum
Lepidoceras chilense
100/1.0/ Colpoon compressum
89/.99/80
Rhoiacarpos capensis
Nestronia umbellula
Osyris lanceolata
Osyris quadripartita
Exocarpos aphylla
82/1.0/89
Omphacomeria acerba
Exocarpos bidwillii
Mida salicifolia
Nanodea muscosa
Okoubaka aubrevillei
74/.95/80
Scleropyrum pentandrum
99/1.0/79
Staufferia capuronii
Pilgerina madagascariensis
Pyrularia pubera
Acanthosyris asipapote
Acanthosyris falcata
Cervantesia tomentosa
Jodina rhombifolia
76/.78/ Thesium subsucculentum
93/1.0/67
Thesium fragile
Thesium chinense
75/.65/ Thesium fruticosum
Osyridicarpos schimperianus
Buckleya distichophylla
Comandra umbellata
Geocaulon lividum
Cansjera leptostachya
Urobotrya siamensis
Opilia amentacea
64/1.0/79
Pentarhopalopilia marquesii
69/1.0/73
Champereia manillana
Agonandra macrocarpa
Anthobolus leptomerioides
Lepionurus sylvestris
56/ - / -
Amphorogynaceae
Viscaceae
-/.59/ -
Santalaceae
Nanodeaceae
Cervantesiaceae
Thesiaceae
Comandraceae
Opiliaceae
0.01 substitutions/site
496
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TAXON 64 (3) • June 2015: 491–506
tree) were not well supported. Because the plastid genes are
absent in Balanophoraceae, this partition could not be used to
assess its position in the order (Fig. 2). For the four non-plastid
genes (Fig. 2), a monophyletic family was not supported and the
same topology and clades (A and B) as were seen on the 7-gene
concatenated tree (Fig. 1) were obtained in the ML analysis.
Conversely, Balanophoraceae was resolved as monophyletic,
albeit weakly (MPBS = ca. 50%) on the MP tree (Fig. 2; Electr.
Suppl.: Fig. S2). Exclusion of the third-codon position of matR
and RPB2 from the 4-gene non-plastid partition yielded similar
results for the position of Balanophoraceae (Electr. Suppl.: Fig.
S5). This exercise removed much of the phylogenetic signal,
thus support for some of the relationships along the “spine” of
the tree was reduced, particularly in the in the MP tree. For the
ML tree, the same topology as seen in Fig. 2 was recovered.
Results of the SOWH test suggest that ML rejects Balano
phoraceae monophyly. The observed difference in likelihood
for the ML topology and the topology resulting from a search
constrained to return a monophyletic Balanophoraceae was
42.4064. This delta value was much greater than all 100 delta
values for data simulated on the constrained topology (P <
0.01; the largest simulated delta value was 0.0021). However,
the Huelsenbeck test, used to determine whether LBA could be
misleading MP to return a monophyletic Balanophoraceae even
if the true tree had a polyphyletic Balanophoraceae, suggests
that LBA is not misleading MP. Balanophoraceae monophyly
was not recovered in any tree resulting from MP analysis of the
100 datasets simulated on the ML topology (on which Balano
phoraceae was polyphyletic; data not shown).
A Four non-plastid genes
84
ML
52
98
100
74
89
Amphorogynaceae
Viscaceae
Santalaceae
Nanodeaceae
Thesiaceae
Cervantesiaceae
Comandraceae
Opiliaceae
Loranthaceae
MP strict
52
70
98
65
Balanophoraceae B
98
89
100
Schoepfiaceae
Misodendraceae
Fig. 2. Comparisons of tree topologies of Santalales for two gene
partitions using maximum likelihood (ML) and strict consensus
maximum parsimony (MP). Bootstrap support values are shown
above the nodes. A, Trees derived
from four non-plastid genes (SSU
and LSU rDNA, RPB2, matR);
B, trees derived from three plastid
genes (accD, matK, rbcL).
52
62
Balanophoraceae A
Olacaceae
Coulaceae
Ximeniaceae
Octoknemaceae
Aptandraceae
Erythropalaceae
Strombosiaceae
Outgroups
54
79
B Three plastid genes
100
ML
98
82
100
81
77
100
58
98
100
100
59
100
94
Amphorogynaceae
Viscaceae
Santalaceae
Nanodeaceae
Thesieaceae
Comandraceae
Cervantesiaceae
Opiliaceae
Loranthaceae
Schoepfiaceae
Misodendraceae
Octoknemaceae
Coulaceae
Aptandraceae
Ximeniaceae
Olacaceae
Erythropalaceae
Strombosiaceae
Outgroups
100
MP strict
62
92
53
100
100
77
54
79
100
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DISCUSSION
This study represents the first molecular phylogenetic
analysis to use comprehensive taxon sampling in Santalales,
including Balanophoraceae. DNA sequences for 148 of the
total 179 genera in the order were utilized, including 10 of 17
genera of Balanophoraceae. Although plastid genes could not
be PCR-amplified from Balanophoraceae, three genes (rbcL,
matK, accD) were concatenated with nuclear RPB2, SSU and
LSU rDNA and mitochondrial matR to maximize resolution.
With newly generated sequences added to those from previous
studies, resolution of the position of Balanophoraceae within
Santalales has improved.
Relationships among the autotrophic and hemiparasitic
clades of Santalales. — The phylogenetic relationships among
the major clades in Santalales (minus Balanophoraceae) are
generally congruent with those presented in previous molecular
phylogenetic investigations (Der & Nickrent, 2008; Malécot
& Nickrent, 2008; Vidal-Russell & Nickrent, 2008a, b). Each
of these clades will be briefly discussed, particularly with reference to two classifications that have appeared after publication
of the above molecular studies: the Angiosperm Phylogeny
Website (Stevens, 2001–) and Kuijt (2015). The traditionally
recognized family Olacaceae was shown to be polyphyletic by
Malécot & Nickrent (2008) and eight clades were recognized
as families in Nickrent & al. (2010): Strombosiaceae, Erythro
palaceae, Octoknemaceae, Ximeniaceae, Aptandraceae, Coul
aceae, Olacaceae and Schoepfiaceae (Fig. 1). Although interfamilial relationships were not fully resolved, all of these families
were strongly supported by the molecular data.
With its six genera, Strombosiaceae was classified as a
family by Nickrent & al. (2010) and Stevens (2001–) but not by
Kuijt (2015) who lumped these genera, along with Heisteria
Jacq., Maburea Maas, and Brachynema Benth. into a broadly
defined Olacaceae. As discussed in Malécot & Nickrent (2008),
molecular and morphological cladistic trees (Malécot & al.,
2004) have points of agreement and disagreement regarding
relationships within Strombosiaceae. Given that Olacaceae s.l.
(as defined by Kuijt) still shows extreme morphological heterogeneity, we believe it is more prudent to use the molecular data
to inform how to partition this variability in a phylogenetically
meaningful way. Morphological features shared by members
of this family were discussed in Nickrent & al. (2010) and are
presented in more detail in Nickrent (1997–).
The present study includes three genera of Erythropal
aceae: Erythropalum Bl., Heisteria, and Maburea. In addition, the genus Brachynema (not sampled here) was shown
via molecular work by K. Wurdack (unpub.) to belong in this
family, near Maburea. These genera have very similar leaf
anatomy (Maas & al., 1992) and also have axile placentation,
absent elsewhere in Santalales. Morphological features that
support placing Brachynema in Santalales include the presence
of a valvate perianth and an acrescent calyx. If Brachynema
truly belongs in this family, then the already wide array of
morphological variation in vegetative and reproductive features
increases further. With regard to Erythropalum, Kuijt (2015)
states “the systematic affinities of Erythropalum have yet to be
498
resolved”, yet both MP and ML trees reported here show strong
support for its inclusion in this family. Kuijt (2015) indicates
he followed Sleumer (1935) in removing Erythropalum from
Santalales; however, a later publication by the same author
includes the genus in Olacaceae (Sleumer, 1980).
The family Octoknemaceae, containing only the genus
Octoknema was recognized by Nickrent & al. (2010), Stevens
(2001–) and Kuijt (2015). Despite adding nuclear and mitochondrial sequence data for Octoknema, its position in Santalales
remains poorly resolved. There appears to be conflict between
the non-plastid and plastid partitions (Fig. 2) where the latter
placed it as weakly supported as sister to the “non-Olacaceae”
clades. This relationship was also seen in Malécot & Nickrent
(2008) which had only two plastid genes (rbcL, matK) available for analysis. Although the tree inferred from RPB2 plus
SSU rDNA agreed with this placement, the tree resulting from
matR did not, thus leaving the placement of Octoknemaceae
ambiguous.
Ximeniaceae composed of Curupira Black, Douradoa
Sleumer (not sampled here), Malania Chun & Lee, and Ximenia L. is a well-supported clade from both molecules and
morphology. The family was recognized as composed here
by Nickrent & al. (2010), Stevens (2001–) and Kuijt (2015). Its
position in the Santalales phylogeny is variable depending
upon the gene or method of analysis, often forming a weakly
supported clade with Coulaceae (Fig. 1A; Electr. Suppl.: Figs.
S1, S2). For Ximenia, positive evidence exists for root parasitism (DeFilipps, 1969); however, haustoria could not be seen on
excavated roots of a large individual of Curupira (C. Clement,
pers. comm.) nor on potted seedlings (Rodrigues, 1961). If some
Ximeniaceae are parasitic and others are not, then it is possible
that parasitism evolved more than once in the order. Alternatively, it may have evolved only once, but was then lost in some
Ximeniaceae. The loss of parasitism once it has evolved in a
lineage has never been documented and, given the selective
advantage this trophic mode provides, this explanation seems
less likely. Finally, it is possible that with additional searching,
especially on young roots of older plants growing in the presence of host roots, haustoria will be found. Clearly additional
basic research is required.
Aptandraceae was recognized as a family by Nickrent
& al. (2010), Stevens (2001–) and in a modified form by Kuijt
(2015). The topology of this clade (Fig. 1) and the one derived
from a 4-gene analysis (Ulloa & al., 2010) were identical. The
family is composed of two well-supported clades: the Aptandra clade (Aptandra Miers, Chaunochiton Benth., Harmandia
Baillon, Hondurodendron Ulloa & al., Ongokea Pierre) and the
Anacolosa clade (Anacolosa Bl., Cathedra Miers, Phanerodiscus Cavaco), both characterized by several morphological synapomorphies (Ulloa & al., 2010). Kuijt (2015) excluded Anacolosa and Cathedra stating these genera “lack such fundamental
features”, referring to anther dehiscence by reflexed valves or
pores. Because he believed these two genera had “more regular anther structure”, and did not describe their dehiscence,
Kuijt (2015) placed them in Olacaceae. The variable anther
morphology in Aptandraceae was discussed in Ulloa & al.
(2010). In fact, the anther dehiscence in Cathedra is similar to
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that seen in Chaunochiton and Phanerodiscus, i.e., porose (see
Aptandraceae images in Nickrent, 1997–). Likewise, the slit or
porose dehiscence is described and illustrated for Anacolosa
in Capuron (1968). Thus, both molecular data and morphology
strongly support recognition of Aptandraceae as circumscribed
by Nickrent & al. (2010).
Coulaceae was circumscribed identically by Nickrent & al.
(2010), Stevens (2001–) and Kuijt (2015). Composed of Coula
Baillon, Minquartia Aublet and Ochanostachys Masters, it is
strongly supported as monophyletic; however, its position in
Santalales is not stable. ML trees for SSU rDNA and matK
(Electr. Suppl.: Fig. S1) as well as the 7-gene ML tree with fast
Balanophoraceae removed (Electr. Suppl.: Fig. S3) show Coul
aceae as sister to Ximeniaceae but this relationship was not
recovered in the 7-gene ML tree with all taxa included (Fig. 1).
Haustoria were not found on excavated roots of Ochanostachys
amentacea Mast. cultivated at the Rimba Ilmu Botanic Garden
in Malaysia (Teo, 1997), thus at least this member of the family
appears to be autotrophic.
Olacaceae s.str. is composed of Dulacia Sleumer, Olax L.,
and Ptychopetalum Benth. which follows Nickrent & al. (2010)
and Stevens (2001–) but not Kuijt (2015). The latter author
did not recognize Erythropalaceae nor Strombosiaceae and
included those members, as well as the above three genera and
Brachynema Benth, in a heterogeneous Olacaceae s.l. composed of 13 genera. Olacaceae s.str. is very well supported as
monophyletic based on molecules and as discussed in Malécot
& Nickrent (2008), have long been recognized for their morphological, anatomical, and palynological homogeneity. Haustorial
parasitism has been documented for Olax (Pate & al., 1990) and
Ptychopetalum (Anselmino, 1932).
The middle portion of the Santalales tree (Fig. 1B) is where
much evolutionary change is taking place. Here is where the
hemiparasites Santalaceae s.l., Misodendraceae, Schoepfi
aceae and Loranthaceae originate, as well as the holoparasites
in Balanophoraceae (discussed below). These clades apparently diverged from “Olacaceae-like” ancestors ca. 90–100 Ma
(Vidal-Russell & Nickrent, 2008b; Bell & al., 2010; Naumann
& al., 2013). Misodendraceae contains one genus, Misodendrum Banks ex DC., with eight species of aerial parasites of
Nothofagus Blume in southern South America (Vidal-Russell
& Nickrent, 2007). Time estimates using Bayesian relaxed
molecular clock methods date the appearance of the family, and
likely the first mistletoes, at ca. 80 Ma (Vidal-Russell & Nickrent, 2008b). This clade diverged from a clade of root parasites classified in Nickrent & al. (2010) as Schoepfiaceae. This
family, composed of Arjona Comm. ex Cav., Quinchamalium
Molina, and Schoepfia Schreber was recognized by Stevens
(2001–) and Kuijt (2015), but the latter author includes only
the genus Schoepfia. The sister relationship between Misodendraceae and Schoepfiaceae received strong support with
most molecular partitions. Moreover, the inclusion of Arjona
and Quinchamalium in Schoepfiaceae is strongly supported by
molecular data and several morphological features discussed in
Nickrent & al. (2010). These data were apparently dismissed by
Kuijt (2015) who retained Arjona and Quinchamalium in their
traditional family, Santalaceae s.l.
The Misodendraceae / Schoepfiaceae clade is sister to
another composed of Loranthaceae and the Balanophoraceae
B clade. This topology is obtained using the full 7-gene dataset
as well as the non-plastid and plastid gene partitions (Figs. 1,
2). Relationships within Loranthaceae are largely congruent
with those previously published (Vidal-Russell & Nickrent,
2008a), hence they will not be described in detail here. The
Australian root parasite Nuytsia is strongly supported as sister to the remainder of the family. Although the major clades,
classified as tribes and subtribes in Nickrent & al. (2010) were
recovered, the “spine” of the Loranthaceae tree has a number
of poorly resolved nodes that will require additional molecular
markers to resolve. That classification was reported verbatim
in Kuijt (2015). Loranthaceae was the last of the five mistletoe
clades to evolve, ca. 28 Ma (Vidal-Russell & Nickrent, 2008b)
and it subsequently underwent a massive adaptive radiation
producing great generic and specific diversity.
The upper portion of the Santalales ML tree (Fig. 1C) contains Opiliaceae and Santalaceae s.l. as presented by Stevens
(2001–). The classification for this group here follows Nickrent
& al. (2010) where Santalaceae s.l. is composed of seven families: Comandraceae, Thesiaceae, Cervantesiaceae, Nanode
aceae, Santalaceae s.str., Viscaceae and Amphorogynaceae.
The classification system of Kuijt (2015) is most similar to that
of Pilger (1935) which contained a broadly defined Santalaceae
as well as Eremolepidaceae and Viscaceae. Kuijt (2015) did
not follow an existing nor propose a new tribal classification
of Santalaceae. Moreover, advancements such as recognition
of Amphorogyneae (Stauffer, 1969) or insights gained from
molecular analyses (Der & Nickrent, 2008) were not incorporated, thus the Santalaceae treatment by Kuijt (2015) is not a
classification but an alphabetical list of generic descriptions.
Opiliaceae is strongly supported as sister to the remaining clades. Although included in Olacaceae by many 19th
century workers, the family Opiliaceae has been consistently
recognized after the treatment by Sleumer (1935). Members
have leaves with cystoliths, bisexual or unisexual flowers, and
a superior ovary with one ovule (Kuijt, 2015). Seven of the
ten genera in this family were sampled as well as the genus
Anthobolus which was traditionally classified in Santalaceae
near Exocarpos Labill. (Stauffer, 1959). As discussed in Der
& Nickrent (2008) and Nickrent & al. (2010), the finding that
Anthobolus is more closely related to Opiliaceae was surprising, although both have a superior ovary which differs from
most Santalaceae s.l. with inferior ovaries. True ovules are seen
in Opiliaceae but not in Anthobolus which has a central coneshaped placenta and undifferentiated ovules (Stauffer, 1959).
With regard to Anthobolus, Kuijt (2015) argued “its affinity
with the Santalaceous Exocarpos is undeniable”. It should be
pointed out, however, that reductions in the placental-ovule
complex in Opiliaceae have occurred. The ovule of Agonandra
is not elevated on a free-central placenta but is basal (Hiepko,
2000). Taking this reduction trend further one can envision
the condition seen in Anthobolus. The phylogenetic placement in Opiliaceae is consistent across nuclear and chloroplast genes and this relationship is seen not only with A. lepto
merioides F.Muell. (sampled here) but also with A. filifolius
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R.Br. (Nickrent, data not shown). It is worth considering that
the morphological similarity to Exocarpos reflects convergence or atavism, as is prevalent in Santalaceae s.l. (Der &
Nickrent, 2008).
The classification of Stevens (2001–) presents Santalaceae
s.l. containing seven tribes or groups that correspond to the
families of Nickrent & al. (2010). It is curious that the rank of
family was accepted for the segregates of Olacaceae s.l. but
was not followed for the equally polyphyletic Santalaceae s.l.
As shown in the present multigene study, both groups have
well-supported clades (here recognized at the familial rank)
and both have poorly supported interrelationships among the
families along the “spine” of the tree. Given the topology
and support values for the nodes in the upper portion of the
Santalales tree, it is not clear why Stevens (2001–) excluded
Opiliaceae from Santalaceae s.l. As outlined in Nickrent & al.
(2010), four secondary principles were followed (in addition
to monophyly), one of which was stability, i.e., minimizing
nomenclatural changes. Both Santalaceae and Viscaceae are
very well-established in the literature, thus retaining these
names causes the least disruption and preserves information
about these clearly defined families. Three of the five remaining families, Amphorogynaceae, Cervantesiaceae and Thesi
aceae are very strongly supported as monophyletic and each is
well characterized morphologically. The remaining two families (Comandraceae, Nanodeaceae) are small, each containing
just two genera. The former was sister to the Cervantesiaceae /
Thesiaceae clade but with only moderate support (Fig. 1C).
Similarly, Nanodeaceae was sister to a clade containing Santalaceae, Amphorogynaceae and Viscaceae but with low support.
It is likely that additional sequences will eventually resolve the
“spine” of the Santalales tree.
Phylogenetic placement of Balanophoraceae within Santalales. — The results of this study confirmed that Balanophor
aceae are derived from within Santalales (Barkman & al., 2007;
Nickrent & al., 2010; Su & Hu, 2012) and showed the presence of two distinct clades with widely differing substitution
rates: a fast-evolving clade A and a relatively slowly evolving
clade B. The MP tree recovered a monophyletic Balanophoraceae, with low support (Fig. 2; Electr. Suppl.: Fig. S2), whereas
the ML tree placed clade B as sister to Loranthaceae (moderate
support) and clade A two nodes deeper on the tree as sister to
the non-Olacaceae s.l. clades (Fig. 1A–B). The data present
here support a non-monophyletic Balanophoraceae, thus indicating that holoparasitism evolved independently two times
in Santalales. Artifactual phylogenetic relationships resulting from LBA (Felsenstein, 1978) were demonstrated with
another holoparasite group, Rafflesiaceae s.l. (Nickrent & al.,
2004) where MP (as opposed to model based methods) was
particularly susceptible. Among-site rate variation is a common
characteristic of sequence evolution that results from different
selective constraints on different sites (Yang & Kumar, 1996).
In contrast to MP, the model-based analyses better accommodate different sequence evolution parameters such as base
substitution heterogeneity and rate variation among nucleotide
sites (Bos & Posada, 2005; Gadagkar & Kumar, 2005; Philippe
& al., 2005). Given the branch lengths in the Balanophoraceae
500
A clade, it is reasonable to expect such systematic error; however, results of the Huelsenbeck test indicate LBA was not
misleading MP. For the three clade B genera, branch lengths
on the phylogram (Fig. 1B) are not particularly long, in fact
comparable to those seen among genera of Viscaceae. Moreover, after the removal of clade A taxa, the position of clade B
in both the ML and MP tree did not change. When third-codon
position of protein-coding genes are removed, which reduced
some degree of substitution bias, the resulting relationships of
both Balanophoraceae clade A and B remained constant (Electr.
Suppl.: Fig. S5). Balanophoraceae clades A and B were also
consistently separated following removal of the fastest evolving category of sites (Electr. Suppl.: Fig. S6) or by using amino
acid sequences of the five protein-coding genes (Electr. Suppl.:
Fig. S7). These results indicate that the Balanophoraceae clades
were not influenced by LBA and that their topologies reflect
actual phylogenetic affinity.
The recognition of at least two groups within Balanophor
aceae is not unprecedented. As mentioned in the Introduction,
Eichler (1867) separated Mystropetalum from the remaining
Balanophoraceae. His association of the latter with Misodendr
aceae and Loranthaceae is amazingly similar to the molecular
phylogenetic results reported here. Harms (1935) proposed
dividing the genera into six subfamilies and this system was
followed in a slightly modified form by Takhtajan (1997) whose
classification included eight families, all split from Balanophor
aceae s.l. Given the type genus occurs in clade A, we retain
that family name Balanophoraceae Rich. (Richard 1822: 429)
in the strict sense for Balanophora and 13 other genera. For
clade B, two family names are available, Mystropetalaceae
Hook.f. (Hooker, 1853: 94) for Mystropetalon and Dactylanth
aceae (Engl.) Takht. (Takhtajan, 1987: 43) for Dactylanthus and
Hachettea. Given earlier date of publication of the former, we
include those three genera in Mystropetalaceae.
Phylogenetic relationships among genera of Balanophor
aceae. — In Mystropetalaceae, Hachettea of New Caledonia is
sister to Dactylanthus of New Zealand and that clade is sister to
Mystropetalon of South Africa. All three of these genera have
comparatively restricted distributions on Gondwanan landmasses. The time of divergence for this clade is approximately
the late Cretaceous, in agreement with Naumann & al. (2013)
who derived a date for the Santalales / Balanophoraceae clade of
109 Ma. The common ancestor, likely a woody root hemiparasite (as in Olacaceae), underwent a radiation that produced the
common ancestor of Opiliaceae / Santalaceae s.l., the first aerial
parasites (Misodendraceae), the first herbaceous perennial root
hemiparasites (Schoepfiaceae – Arjona, Quinchamalium), the
first root parasitic members of Loranthaceae (i.e., Nuytsia,
Atkinsonia), and the holoparasites of Mystropetalaceae. The
ancient ancestor of Mystropetalaceae was likely woody and
hemiparasitic, but evolutionary changes along this branch produced the herbaceous holoparasites we see in the extant genera.
Reductions and losses of floral parts seen in Balanophoraceae
s.str. (below) are not as pronounced in Mystropetalaceae. For
example, a perianth is present on the female flowers of all three
genera (Hansen, 1986; Holzapfel, 2001; Hansen & Kubitzki,
2015). The morphological reductions of the gynoecium and a
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shared Allium type of embryo sac inspired Fagerlind (1948) to
propose a shared ancestry between “Balanophorales” and Visc
aceae / Helixanthera Lour. (Loranthaceae). Morphological and
anatomical features of the haustorium in Mystropetalon were
considered to be similar to Santalales (Weber, 1986). Given
the phylogenetic data, it is now important to determine if such
apparent similarities represent synapomorphies.
Relationships among the genera Balanophoraceae s.str.
are generally concordant with groups recognized in morphology-based classifications (Takhtajan, 1997, 2009; Hansen
& Kubitzki, 2015). Thonningia Vahl. together with Langsdorffia Raddi were placed in Langsdorffieae by Harms and
this tribe was elevated to subfamily by Takhtajan (2009). The
former genus is found in tropical Africa whereas the latter
has a disjunct distribution that includes Madagascar, New
Guinea, and tropical America. Molecular data place Langsdorffia malagasica (Fawc.) B.Hansen as sister to Thonningia
(Nickrent, unpub. data). As reflected in the classification by
Harms (1935), Langsdorffioideae is related to Balanophoroideae (containing just Balanophora). This is borne out by the
molecular data, chemical data such as the storage of balanophorin (as opposed to starch) in the tubers, and morphology where female flowers have one style. With ca. 16 species,
Balanophora is the largest genus in the family and has a wide
distribution from Madagascar to India, Indomalaya, Australia and Pacific islands. It is monoecious or dioecious with
complex male and female inflorescence structure (Eberwein
& al., 2009). The male flowers have a valvate perianth and
anthers fused into a synandrium whereas the female flowers
are the smallest among angioserms composed of as few as
50 cells (Hansen, 1972). The length of the branch leading to
the two Balanophora species (Fig. 1) is exceptionally long,
thereby reflecting the number of substitutional changes that
accompanied the evolutionary trajectory of this genus. The
neotropical genera Lophophytum Schott & Endl. and Ombrophytum Poepp. have long been known to be related (Harms,
1935) and Lathrophytum Eichl. may also be part of this group
(Nickrent, unpub. molecular data). Their female flowers lack
a perianth and have two styles. Another neotropical subfamily, Helosidoideae (Harms, 1935) contains Corynaea Hook.f.,
Helosis Rich. and three paleotropical genera Ditepalanthus
Fagerl., Rhopalocnemis Junghuhn and Exorhopala Steenis
(none sampled here). The latter genus was synonymized with
Helosis by Eberwein & Weber (2004); however, molecular data confirming that these taxa are congeneric does not
yet exist. The New World genus Scybalium Schott & Endl.
placed in its own family Scybaliaceae by Takhtajan (1997)
also belongs near Corynaea and Helosis (Nickrent, unpub.
molecular data), thus supporting the classification of Harms
(1935). The genera Sarcophyte Sparrm. and Chlamydophytum Mildbr. (latter unsampled) occur in tropical Africa and
are characterized by having robust, paniculate male inflorescences. They were placed in subfamily Sarcophytoideae by
Harms (1935) and Sarcophytaceae by Takhtajan (1997). The
molecular data show Sarcophyte as intermediate in position
between the Balanophoroideae / Langsdorffioideae clade and
the Lophophytoideae / Helosidoideae clade.
Conclusions. — For the autotrophic and hemiparasitic
members of Santalales, this study confirms the composition
of and support for clades seen in previous molecular phylogenetic studies that were classified at the family level. Presented
here is strong evidence that the holoparasitic family Balanophoraceae are derived from within Santalales. A relatively
slow-evolving clade composed of Dactylanthus, Hachettea,
and Mystropetalon (all Southern Hemisphere taxa) was shown
to be sister to Loranthaceae and is here recognized as Mystropetalaceae. The other fast-evolving clade, composed of seven
sampled genera, including Balanophora, has a wide distribution in tropical and subtropical areas and is here recognized
as Balanophoraceae s.str. Our data, which support the nonmonophyly of Balanophoraceae s.l., help to explain why the
morphology-based classifications of this family have historically varied widely.
ACKNOWLEDGEMENTS
This work was supported by the research grants from National
Science Council, Taiwan to JMH (NSC 99-2311-B002-003-MY2). We
thank Dr. Laco Mucina, Dr. Dianne Owen, Dr. Romina Vidal Russell,
Dr. Miguel Angel García, Dr. Valéry Malécot, Dr. Ana Maria Gonzalez,
Dr. Yi-Gang Wei, Dr. Claude dePamphilis, Dr. James Leebens-Mack,
and Marcos Caraballo-Ortiz who helped in obtaining samples and/or
generated sequences of Santalales. We also thank Harvard University
for providing herbarium samples and Royal Botanic Gardens Kew for
providing plant DNA. Finally, we thank an anonymous reviewer who
pointed out the important early work by A.W. Eichler.
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Su & al. • Phylogenetic relationships of Santalales
TAXON 64 (3) • June 2015: 491–506
Appendix 1. Samples used in the phylogenetic analyses. Following each species name is country of origin, collector & number, herbarium of voucher, DNA
accession number and GenBank numbers in the following order: SSU rDNA, LSU rDNA, RPB2, rbcL, matK, accD, and matR. Sequences being reported
here for the first time are indicated by *. Missing sequences are indicated by a dash (–). See Electronic Supplement 2 to view these data in tabular form.
Acanthosyris asipapote M.Nee: Bolivia, M. Nees & I. Vargas 45009 (NY), DLN 4051, DQ329163, AF181776, –, DQ329171, DQ329182, DQ329193, –. Acantho
syris falcata Griseb.: Bolivia, M. Nees 46690 (NY), DLN 4053, DQ329164, –, –, DQ329172, DQ329183, DQ329194, –. Actinanthella menyharthii (Engl. &
Schinz) Balle: Zimbabwe, D. Wiens 4638 (MO), DLN 4375, EU544313, EU544352, –, –, EU544408, –, –. Aetanthus noduosus (Desr.) Engl.: Ecuador, F.M.
Garmendia 1227 (MO), DLN 4561, EU544314, –, –, –, EU544409, –, –. Agelanthus sansibarensis (Engl.) Polhill & Wiens: Kenya, S.A. Robertson s.n. (SIU),
DLN 2987, U59946, EU544353, –, EU544464, EU544410, –, –. Agonandra macrocarpa L.O.Williams: Costa Rica, D.L. Nickrent 2764 (SIU), DLN 2764,
L24079, DQ790205, –, DQ790130, DQ790169, DQ790237, –. Alepis flavida (Hook.f.) Tiegh.: New Zealand, B. Molloy s.n. (SIU), DLN 2743, L24139, EF464474,
–, –, EF464508, *KP263290, –. Amphorogyne celastroides Stauffer & Hürl.: New Caledonia, G.D. McPherson 18051 (MO), DLN 4564, EF584571, –, *KP263324,
–, EF584614, –, –. Amyema glabra (Domin) Danser: Australia, D.L. Nickrent 2795 (SIU), DLN 2795, AF039073, EU544354, –, EU544465, EU544411, –,
(AY453106). Amyema queenslandica (Blakely) Danser: Australia, D.L. Nickrent 2788 ( SIU), DLN 2788, EU544315, EU544355, –, –, EU544412, –, –. Amy
lotheca duthiana (King) Danser: Malaysia, D.L. Nickrent 4022 (SIU), DLN 4022, EU544316, EU544356, –, –, EU544413, –, –. Anacolosa papuana Schellenb.:
Solomon Islands; Indonesia, R. Regalado & M.Q. Sirikolo 692; A.C. Church 338 (MO; A), DLN 4247; Hu 1852, DQ790104, –, (*KP263325), DQ790144,
DQ790181, DQ790250, –. Anthobolus leptomerioides F.Muell.: Australia, B.J. Lepschi & L.A. Craven 4352 (CANB), DLN 4311, EF584572, –, –, EF584589,
EF584615, *KP263291, –. Antidaphne viscoidea Poepp. & Endl.: Costa Rica, S. Sargent s.n. (SIU), DLN 2730, L24080, *KP263237, –, L26068, EF464500,
*KP263292, –. Aptandra tubicina (Poepp.) Benth. ex Miers: Peru, H. van der Werff & R. Vasquez 13846 (MO), DLN 4202, DQ790105, DQ790217, –, DQ790141,
DQ790178, DQ790247, –. Arceuthobium verticilliflorum Engelm.: Mexico, D.L. Nickrent 2065 (SIU), DLN 2065, L24042, EF464470, (AY566624), L26067,
–, –, –. Arjona tuberosa Cav.: Argentina, V. Melzheimer s.n.; Pisann 3594 (SIU; GH), DLN 4131; Hu 1860, EF464468, EF464480, *KP263326, EF464532,
EF464513, –, *KP263264. Atkinsonia ligustrina (Lindl.) F.Muell.: Australia, D. Watson 4458 (SIU), DLN 4343, EF464464, EF464475, –, EF464526, DQ787444,
–, . Bakerella sp.: Madagascar, S. Razafimandimbison 332 (MO), DLN 4161, EU544318, EU544358, –, EU544466, EU544415, –, . Balanophora fungosa
J.R.Forst. & G.Forst.: Australia; Taiwan, D.L. Nickrent 2825; J.-Y. Huang 20040203 (SIU; TAI), DLN 2825; Su 118, JN392868, *KP263238, JQ613269, –, –, –,
JQ613244. Balanophora laxiflora Hemsl.: Taiwan, H.-J. Su 043, 044 (TAI), Su 043, 044, JN392870, *KP263239, JQ613270, –, –, –, JQ613245. Baratranthus
axanthus (Korth.) Miq.: Malaysia, D.L. Nickrent 4029 (SIU), DLN 4029, EU544317, EU544357, –, –, EU544414, –, –. Benthamina alyxifolia (Benth.) Tiegh.:
Australia, W. Forstreuter Be.al.01 (SIU), DLN 4127, EU544319 , EU544359, –, –, EU544416, –, –. Berhautia senegalensis Balle: Gambia, M. Jones s.n. (SIU),
DLN 4576, EU544320, EU544360, –, –, EU544417, –, –. Buckleya distichophylla (Nutt.) Torr.: U.S.A., L.J. Musselman s.n. (SIU), DLN 2735, X16598, EF464473,
–, DQ329180, DQ329191, DQ329202, (DQ110331). Cansjera leptostachya Benth.: Australia, D.L. Nickrent 2815 (SIU), DLN 2815, L24084, DQ790204, –,
DQ790128, DQ790167, –, –. Cathedra acuminata (Benth.) Miers: Brazil, J.A. Ratter & al. 6782 (MO), DLN 4244, FJ848847, –, –, DQ790145, DQ790182,
DQ790251, –. Cecarria obtusifolia Merr.: Australia, B. Hyland 16493 (QRS), DLN 4562, EU544321, EU544361, –, EU544467, EU544418, –, –. Cervantesia
tomentosa Ruiz & Pav.: Bolivia, L.J. Dorr & L.C. Barnett 6941 (MO), DLN 4273, DQ329165, *KP263240, *KP263327, DQ329173, DQ329184, DQ329195,
(DQ110333). Champereia manillana (Blume) Merr.: Thailand, W. Forstreuter s.n. (SIU), DLN 3014, JQ613223, –, JQ613271, DQ790129, DQ790168, DQ790236,
JQ613247. Chaunochiton kappleri (Sagot ex Engl.) Ducke: Costa Rica, N. Zamora & al. 1928 (MO), DLN 3052, DQ790106, DQ790218, –, DQ790142, DQ790179,
DQ790248, –. Choretrum pauciflorum A.DC.: Australia, B. Lepschi & al. 4237 (CANB), DLN 4222, EF584573, –, –, EF464522, EF464503, *KP263293, –.
Cladocolea gracilis Kuijt: Mexico, A.C. Sanders & P.A. Fryxell 4172 (MO), DLN 3066, EU544322, EU544362, –, –, EU544419, –, –. Colpoon compressum
P.J.Bergius: South Africa, D.L. Nickrent 4084 (SIU), DLN 4084, EF584574, –, –, EF584590, EF584616, *KP263294, –. Comandra umbellata (L.) Nutt.: U.S.A.,
G. Tonkovitch s.n. (SIU), DLN 2739, L24772, DQ329170, *KP263241, *KP263328, DQ329181, DQ329192, DQ329203, –. Corynaea crassa Hook.f.: Costa Rica,
D.L. Nickrent & S.-C. Hsiao 3011 (SIU), DLN 3011, L24400, *KP263242, *KP263329, –, –, –, *KP263265. Coula edulis Baill.: Gabon, J.J. Wieringa 3295
(WAG), DLN 3079, –, –, –, DQ790147, DQ790184, DQ790253, –. Curupira tefeensis G.A.Black: Brazil, C. Clement s.n. (INPA), DLN 4988, DQ790107,
DQ790221, , DQ790150, DQ790187, DQ790256, –. Dactylanthus taylorii Hook.f.: New Zealand, C. Ecroyd s.n. (SIU), DLN 4071, AY957443, *KP263243,
*KP263330, –, –, –, AY957447. Dactyliophora novae-guineae (F.M.Bailey) Danser: Australia, B. Hyland 16461 (QRS), DLN 4563, EU544323, EU544363, –,
–, EU544420, –, –. Daenikera corallina Hürl. & Stauffer : New Caledonia, J. Munzinger 2054 (NOU), DLN 4876, EF464462, EF464472? or Josh, *KP263331,
EF464523, EF464504, *KP263295, –. Decaisnina triflora (Span.) Tiegh.: Papua New Guinea, D.L. Nickrent 4491 (WAU), DLN 4491, EU544324, EU544364,
–, EU544468, EU544421, –, –. Dendromyza ledermannii (Pilg.) Stauffer: Papua New Guinea, D.L. Nickrent 4466 (WAU), DLN 4466, EF464463, –, –, EF464524,
EF464505, *KP263297, –. Dendropemon caribaeus Krug & Urb.: Puerto Rico, D.L. Nickrent 2172 (SIU), DLN 2172, AF039075, EU544365, (*KP263332),
EU544469, EU544422, (*KP263296), –. Dendrophthoe curvata (Blume) Miq.: Malaysia, D.L. Nickrent 4012 (SIU), DLN 4012, EU544325, EU544367, –,
(HQ317760), EU544424, –, –. Dendrophthoe longituba (Elmer) Danser: Malaysia, D.L. Nickrent 4010 (SIU), DLN 4010, (HQ317760), EU544366, –, –,
EU544423, –, (DQ110337). Dendrophthora clavata (Benth.) Urb.: Colombia, M. Melampy s.n. (SIU), DLN 2182, L24086, AF181813, –, L26069, EF584636, –,
–. Dendrotrophe varians (Blume) Miq.: Australia; Malaysia, D.L. Nickrent 2827; 4014 (SIU), DLN 2827; DLN 4014, L24087, –, –, EF464520, EF464501, –, –.
Desmaria mutabilis (Poepp. & Endl.) Tiegh. ex T.Durand & B.D.Jacks.: Chile, G. Amico s.n. (SIU), DLN 4510, EF464465, EF464476, –, EF464527, EF464509,
*KP263298, –. Diogoa zenkeri Exell & Mendonça: Gabon, J.J. Wieringa 3288 (WAG), DLN 3078, DQ790108, DQ790223, *KP263333, DQ790152, DQ790189,
DQ790258, *KP263266. Diplatia furcata Barlow: Australia, D.L. Nickrent 2824 (SIU), DLN 2824, L24088, EU544368, –, –, EU544425, –, –. Dufrenoya
sphaerocarpa (Danser) Stauffer: Indonesia, G.G. Hambali s.n. (SIU), DLN 2754, AF039071, –, –, EF584592, EF584617, *KP263299, –. Dulacia candida
(Poepp.) Kuntze: Ecuador, M.J. Macía & al. 553 (MO), DLN 4245, DQ790109, –, *KP263334, DQ790137, DQ790174, DQ790244, DQ110338. Emelianthe
panganensis (Engl.) Danser: Tanzania, E. Mboya 594 (MO), DLN 4889, EU544326, EU544369, –, –, EU544426, –, –. Englerina ramulosa (Sprague) Polhill
& Wiens: Kenya, S.A. Robertson s.n. (SIU), DLN 2984, (L24140), EU544370, –, EU544470, EU544427, –, –. Engomegoma gordonii Breteler: Equatorial
Guinea, B. Senterra 18-81 (P), DLN 4555, DQ790110, –, –, DQ790153, –, –, –. Erianthemum dregei (Eckl. & Zeyh.) Tiegh.: Kenya, S.A. Robertson s.n. (SIU),
DLN 2985, L25679, EU544371, –, –, EU544428, –, –. Erythropalum scandens Blume: Indonesia; China, M. Chase 1328; H.-J. Su 055 (K; TAI), DLN 4165; Su
055, DQ790111, DQ790233, *KP263335, DQ790164, DQ790200, DQ790267, *KP263267. Eubrachion ambiguum (Hook. & Arn.) Engl.: Puerto Rico, D.L.
Nickrent 2699 (SIU), DLN 2699, L24141, AF389273, –, L26071, EF464498, *KP263300, –. Exocarpos aphyllus R.Br.: Australia, A. Markey & B. Barlow s.n.
(SIU), DLN 3094, EF584575, –, –, EF584593, EF584618, *KP263301, –. Exocarpos bidwillii Hook.f.: New Zealand, B. Molloy s.n. (SIU), DLN 2745, L24142,
*KP263244, (*KP263336), EF584594, EF584619, *KP263302, –. Gaiadendron punctatum (Ruiz & Pav.) G.Don: Costa Rica, S. Sargent s.n. (SIU), DLN 2729,
L24143, DQ790209, –, L26072, DQ787445, DQ790238, DQ110339. Geocaulon lividum (Richardson) Fernald: U.S.A., J. Fetzner s.n. (SIU), DLN 3047, AF039072,
*KP263245, –, EF584595, EF584620, *KP263303, –. Ginalloa arnottiana Korth.: Malaysia, J. Beaman 9074 (SAR), DLN 2982, L24144, –, –, L26070, EF584637,
–, –. Globimetula dinklagei (Engl.) Danser: Gabon, J.J. Wieringa 2858 (WAG), DLN 3087, AF039076, EU544372, –, –, EU544429, –, –. Hachettea austro
caledonica Baill.: New Caledonia, J.-M. Groult s.n. (SIU), DLN 4181, AY957444, *KP263246, *KP263337, –, –, –, AY957448. Harmandia mekongensis Baill.:
Indonesia, Koizumi 1411 (KYO), DLN 5597, FJ848849, –, –, FJ848842, FJ848845, FJ848843, –. Heisteria acuminata (Humb. & Bonpl.) Engl.: Panama, R. Perez
161835 (US), STRI:BCI 161835, –, –, –, GQ981760, GQ982009, –, –. Heisteria cauliflora Sm.: French Guyana, M.F. Prévost 3796 (CAY), DLN 4254, DQ790112,
DQ790229, –, DQ790160, DQ790196, DQ790264, –. Heisteria concinna Standl.: Panama, C. Augspurger s.n. (SIU), DLN 2732, L24146, DQ790230, *KP263338,
DQ790161, DQ790197, –, –. Heisteria densifrons Engl.: French Guyana, J.K. Munzinger & al. 497 (P), DLN 4232, DQ790113, DQ790231, –, DQ790162,
DQ790198, –, –. Heisteria parvifolia Sm.: Cameroon, M. Cheek 5985 (K), DLN 4166, –, DQ790232, –, AJ131771, AY042600, DQ790266, GU351220. Helix
anthera coccinea (Jack) Danser: Malaysia, D.L. Nickrent 4019 (SIU), DLN 4019, –, EU544373, –, –, EU544430, –, –. Helixanthera cylindrica (Jack ex Roxb.)
Danser: Malaysia, C. Calvin & al. B22 (SAR), DLN 4037, EU544327, EU544374, –, –, EU544431, –, –. Helosis cayennensis (Sw.) Spreng.: Costa Rica, D.L.
Nickrent & S.-C. Hsiao 3006; J. Gomez s.n. (SIU), DLN 3006; DLN 3017, L25682, *KP263247, –, –, –, –, *KP263268. Hondurodendron urceolatum C.Ulloa,
504
Version of Record
Su & al. • Phylogenetic relationships of Santalales
TAXON 64 (3) • June 2015: 491–506
Appendix 1. Continued.
Nickrent, Whitef. & D.L.Kelly: Honduras, Fagen & al. DA/2MS 313 (MO), DLN 5555, FJ848848, , –, FJ848841, FJ848846, FJ848844, –. Ileostylus micranthus
Tiegh.: New Zealand, B. Molloy s.n. (SIU), DLN 2741, EU544329, EU544376, –, EU544471, EU544433, –, –. Jodina rhombifolia (Hook. & Arn.) Reissek:
Bolivia, M. Nees 46673 (NY), DLN 4052, DQ329166, –, –, DQ329174, DQ329185, DQ329196, –. Korthalsella lindsayi (Oliv. ex Hook.f.) Engl.: New Zealand;
Taiwan, B. Molloy s.n.; C.-C. Wu s.n. (SIU; TAI), DLN 2740; Su 119, L24150, (*KP263248), (*KP263339), L26073, –, –, –. Lepeostegeres lancifolius Danser:
Malaysia, Calvin & al. B27 (SAR), DLN 4041, –, EU544379, –, –, EU544435, –, –. Lepidaria forbesii Tiegh.: Malaysia, D.L. Nickrent 4044 (SIU), DLN 4044,
EU544330, EU544378, –, –, EU544434, –, –. Lepidoceras chilense (Molina) Kuijt: Chile, C. Marticorena & R. Rodríguez 10043 (CONC), DLN 4065, EF464459,
–, –, EF464519, EF464499, –, –. Lepionurus sylvestris Blume: Indonesia; unknown, G. Hambali s.n.; M.W. Chase 1333 (SIU; K), DLN 2880; Kew DNA Bank
1333, DQ790101, DQ790206, *KP263340, DQ790131, DQ790170, –, *KP263269. Leptomeria aphylla R.Br.: Australia, B.J. Lepschi 4875 (CANB), DLN 4609,
–, –, –, EF584597, EF584622, *KP263305, –. Leptomeria pauciflora R.Br.: Australia, A. Markey & B. Barlow s.n. (SIU), DLN 3081, EF464460, EF464471, –,
EF464521, EF464502, –, –. Ligaria cuneifolia (Ruiz & Pav.) Tiegh.: Chile, G. Amico s.n. (SIU), DLN 4567, L24152, EF464477, –, EF464528, EF464510, –, –.
Lophophytum leandrii Eichler : Argentina, M. Gonzalez 291 (TAI), Gonzalez 291, *KP263283, *KP263249, *KP263341, –, –, –, *KP263270. Loranthus
delavayi Tiegh.: Taiwan, C.-C. Wu 0033 (TAI), Wu 0033, JQ613220, –, –, HQ317767, –, –, JQ613248. Loranthus europaeus Jacq.: Italy, U. Kuhlmann s.n.
(SIU), DLN 2849, L24153, EU544380, –, JQ933393, EU544436, –, –. Loranthus kaoi (J.M.Chao) H.S.Kiu: Taiwan, H.-J. Su 021 (TAI), Su 021, JQ613221, –,
JQ613272, –, *KP263261, –, JQ613249. Loxanthera speciosa Blume: Malaysia, D.L. Nickrent 4026 (SIU), DLN 4026, EU544332, EU544382, –, –, EU544437,
–, –. Lysiana filifolia Barlow: Australia, D.L. Nickrent 4449 (SIU), DLN 4449, EU544333, EU544383, –, –, EU544438, –, –. Maburea trinervis Maas: Guyana,
R. Zagt s.n. (P), DLN 4256, DQ790114, DQ790234, *KP263342, DQ790165, DQ790201, DQ790268, DQ110345. Macrosolen cochinchinensis (Lour.) Tiegh.:
Malaysia; China, C.Calvin & al. s.n.; H.-J. Su 052 (SAR; TAI), DLN 4038; Su 052, EU544334, EU544384, *KP263343, *KP263282, EU544439, –, *KP263271.
Malania oleifera Chun & S.K.Lee: China, Caoming 0340; H.-J. Su 051 (P; TAI), DLN 4158; Su 051, DQ790115, DQ790222, *KP263344, DQ790151, DQ790188,
DQ790257, *KP263272. Mida salicifolia A.Cunn.: New Zealand, C.C. Ogle 3413 (CHR), DLN 4233, EF584577, –, *KP263345, EF584598, EF584623, *KP263306,
*KP263273. Minquartia guianensis Aubl.: Costa Rica, D.L. Nickrent 2758 (SIU), DLN 2758, L24396, –, *KP263346, DQ790148, DQ790185, DQ790254,
DQ110346. Misodendrum linearifolium DC.: Chile, G. Amico 136 (BCRU), DLN 4591, L24397, DQ790211, –, L26074, DQ787438, –, –. Misodendrum
punctulatum Banks ex DC.: Argentina, R. Vidal-Russell 61, 62 (BCRU), Su 117, *KP263284, *KP263250, *KP263347, EF464531, DQ787443, (*KP263307),
*KP263274. Moquiniella rubra A.Spreng.: South Africa, K. Steiner 2836 (NBG), DLN 3042, AF039078, DQ790207, –, DQ790132, DQ790171, –, –. Muel
lerina eucalyptoides (DC.) Barlow: Australia, D. Watson s.n. (SIU), DLN 4310, EU544335, EU544385, –, EU544472, EU544440, –, –. Myoschilos oblongum
Ruiz & Pav.: Chile, M.F. Gardner & S.G. Knees 4387 (MO), DLN 4182, EF584578, –, –, EF584599, EF584624, *KP263308, –. Mystropetalon thomii Harv.:
South Africa, D.L. Nickrent 4091 (SIU), DLN 4091, AY957445, *KP263251, *KP263348, –, –, –, AY957449. Nanodea muscosa Banks ex C.F.Gaertn.: Argentina, D.M. Moore 2302 (MO), DLN 4183, EF584579, –, –, EF584600, EF584625, *KP263309, –. Nestronia umbellula Raf.: U.S.A., L.J. Musselman s.n. (SIU),
DLN 2736, L24399, –, –, EF584601, EF584626, *KP263310, DQ110348. Notanthera heterophylla (Ruiz. & Pav.) G.Don.: Chile, C. Aeodo 7202 (MA), DLN
4372; 4582, EF464466, EF464478, –, EF464529, EF464511, –, –. Notothixos subaureus Oliv.: Australia, D.L. Nickrent 2790 (SIU), DLN 2790, L24403,
*KP263252, –, L26075, –, (*KP263311), . Nuytsia floribunda R.Br.: Australia, B. Lamont s.n.; A. Markey & B. Barlow; L. Mucina s.n. (SIU; TAI), DLN 2747;
DLN 3080; Su 120, DQ790103, DQ790210, *KP263349, DQ790134, DQ787446, DQ790239, DQ110349. Ochanostachys amentacea Mast.: Indonesia, M. Chase
1329 (K), DLN 4167, DQ790116, –, –, DQ790146, DQ790183 , DQ790252, –. Octoknema sp.: Equatorial Guinea, B. Senterra SO 291 (P), DLN 4560, *KP263285,
–, *KP263350, DQ790139, DQ790176, –, *KP263275. Oedina pendans (Engl. & K.Krause) Polhill & Wiens: Tanzania, R.E. Gereau & C.J. Kayombo 4213
(MO), DLN 4329, EU544336, EU544386, –, –, EU544441, –, –. Okoubaka aubrevillei Pellegr. & Normand: Cameroon, M. Cheek 6007 (K), DLN 4173, –, –,
–, DQ329175, DQ329186, DQ329197, –. Olax emirnensis Baker: Madagascar, G.E. Schatz & al. 3620 (MO), DLN 4035, DQ790119, DQ790214, –, DQ790136,
DQ790173, DQ790243, . Olax imbricata Roxb.: China, J.-M. Hu 1618 (TAI), Hu 1618, JQ613222, *KP263253, *KP263351, , –, –, JQ613246. Olax aphylla
R.Br.: Australia, D.L. Nickrent 2810 (SIU), DLN 2810, L24405, DQ790212, –, DQ792943, –, DQ790241, –. Olax benthamiana Miq.: Australia, M. Chase 2176
(K), DLN 4168, DQ790118, DQ790213, –, DQ790135, AY042620, DQ790242, –. Oliverella rubroviridis Tiegh.: Zambia, N.B. Zimba & al. 1097 (MO), DLN
4330, EU544337, EU544387, –, –, EU544442, –, –. Ombrophytum subterraneum (Aspl.) B.Hansen: Chile, J.D. Mauseth 1987-506 (TEX), DLN 2983, L24406,
*KP263254, –, –, , –, EU281127. Omphacomeria acerba (R.Br.) A.DC.: Australia, B. Lepschi & B.R. Murray 4213 (CANB), DLN 4221, EF584580, –, –,
EF584602, EF584627, *KP263312, –. Oncella ambigua (Engl.) Tiegh.: Kenya, S.A. Robertson & K. Medley 5459 (MO), DLN 4673, EU544338, –, –, –, EU544443,
–, –. Oncocalyx sulfureus (Engl.) Wiens & Polhill: Kenya, W. Forstreuter 9117 (SIU), DLN 2850, EU544339, EU544388, –, –, EU544444, –, –. Ongokea gore
(Hua) Pierre: Gabon, F.J. Breteler & al. 14888 (WAG), DLN 4184, DQ790120, DQ790216, *KP263352, DQ790140, DQ790177, DQ790246, DQ110350. Opilia
amentacea Roxb.: Australia, D.L. Nickrent 2816 (SIU), DLN 2816, L24407, DQ790202, –, L26076, AY042621, *KP263313, –. Oryctanthus occidentalis (Kunth)
Kuijt: Costa Rica, D.L. Nickrent 2763 (SIU), DLN 2763, L24408, EU544389, –, –, EU544445, –, –. Osyridicarpos schimperianus (Hochst. ex A.Rich.) A.DC.:
South Africa, D.L. Nickrent 4110 (SIU), DLN 4110, EF584581, , –, EF584603, EF584628, *KP263315, –. Osyris lanceolata Hochst. & Steud.: South Africa,
D.L. Nickrent 2731 (SIU), DLN 2731, U42803, AF389274, –, EF464525, EF464506, –, –. Osyris quadripartita Salzm. ex Decne.: Spain, D.L. Nickrent 4062
(SIU), DLN 4062, EF584582, (FJ588878), –, EF584604, AY042623, *KP263314, (AF520155). Passovia pyrifolia (Kunth) Tiegh.: Costa Rica, D.L. Nickrent
2762 (SIU), DLN 2762, L24412, EU544392, –, –, EU544448, –, –. Pentarhopalopilia marquesii (Engl.) Hiepko: Gabon, J.J.F.E. deWilde & R.W. deWildeBakhuizen 11212 (WAG), DLN 4180, DQ790102, DQ790203, –, DQ790127, DQ790166, –, –. Peraxilla tetrapetala (L.f.) Tiegh.: New Zealand, B. Molloy s.n.
(SIU), DLN 2744, EU544340, EU544390, –, EU544473, EU544446, *KP263316, –. Phacellaria rigidula Benth.: China, Y. Ding s.n. (SIU), DLN 5042, EF584583,
–, –, EF584605, (EF584629), –, –. Phanerodiscus capuronii Malécot, G.E.Schatz & Bosser: Madagascar, G.E. Schatz & al. 3439 (MO), DLN 4204; Kew DNA
Bank 9294, DQ790122, DQ790219, (*KP263353), DQ790143, DQ790180, DQ790249, –. Phoradendron californicum Nutt.: U.S.A., J. Paxton s.n. (SIU), DLN
2689, AF039070, AF181803, –, EF584613, EF584639, –, –. Phoradendron leucarpum (Raf.) Reveal & M.C.Johnst.: U.S.A., D.L. Nickrent 2077 (ILL), DLN
2077, X16607, *KP263256, *KP263354, GQ997750, GQ997723, GQ997713, –. Phragmanthera crassicaulis (Engl.) Balle: Gabon, J.J. Wieringa 2506 (WAG),
DLN 3037, EU544341, EU544391, –, –, EU544447, –, –. Pilgerina madagascariensis Z.S.Rogers, Nickrent & Malécot: Madagascar, R. Rabevohitra & al. 4485
(MO), DLN 4954, DQ329169, –, –, DQ329178, DQ329189, DQ329200, –. Plicosepalus sagittiflorus (Engl.) Danser: Kenya, W. Forstreuter s.n. (SIU), DLN
2852, EU544342, EU544393, –, –, EU544449, –, –. Psittacanthus calyculatus A.C.Sm.: Mexico, D. Wiens s.n. (SIU), DLN 4043, (L24414), EU544394, –, –,
EU544450, –, –. Ptychopetalum petiolatum Oliv.: Gabon, F.J. Breteler 14745 (WAG), DLN 4212, DQ790121, DQ790215, *KP263355, DQ790138, DQ790175,
DQ790245, –. Pyrularia pubera Michx.: U.S.A., L.J. Musselman s.n. (SIU), DLN 2737, L24415, –, –, DQ329179, EF464507, DQ329201, –. Quinchamalium
chilense Molina: Argentina; Bolivia, R. Vidal-Russell s.n.; J.R.I. Wood 9149 (SIU; K), DLN 4503; Kew DNA Bank 9573, EF464469, *KP263257, *KP263356,
EF464533, EF464514, *KP263317, *KP263276. Rhoiacarpos capensis (Harv.) A.DC. : South Africa, D.L. Nickrent 4117 (SIU), DLN 4117, EF584584, –, ,
EF584606, EF584630, *KP263318, –. Santalum album L.: India; Taiwan, R. Narayana s.n.; H.-J. Su 028 (SIU; TAI), DLN 2734; Su 028, JQ613224, AY957453,
JQ613266, L26077, *KP263262, *KP263319, JQ613250. Santalum macgregorii F.Muell.: Papua New Guinea, D.L. Nickrent 4499 (WAU), DLN 4499, EF584585,
–, –, EF584607, EF584631, –, –. Sarcophyte sanguinea Sparrm.: South Africa, D.L. Nickrent 4109 (SIU), DLN 4109, *KP263286, *KP263258, –, –, –, –,
*KP263277. Schoepfia chinensis Gardner & Champ.: China, H.-J. Su 054 (TAI), Su 054, *KP263287, –, *KP263357, HQ415145, *KP263263, –, *KP263278.
Schoepfia jasminodora Siebold & Zucc.: Taiwan, H.-J. Su 022 (TAI), Su 022, JQ613226, –, JQ613273, HQ415146, HQ415321, –, JQ613252. Schoepfia schre
beri J.F.Gmel.: Bahamas, D.L. Nickrent 2599 (ILL), DLN 2599, L24418, AF389261, –, L11205, AY957451, DQ790240, GU351300. Scleropyrum pentandrum
(Dennst.) Mabb.: Thailand, S. Suddee & al. 1007 (TCD), DLN 4347, DQ329167, –, –, DQ329176, DQ329187, DQ329198, –. Scorodocarpus borneensis (Baill.)
Becc: Malaysia, S.P. Teo s.n.; M.W. Chase 1331 (SIU; K), DLN 3028; Kew DNA Bank 1331, U59934, DQ790228, *KP263358, DQ790159, DQ790195, DQ790263,
*KP263279. Scurrula ferruginea (Jack) Danser: Malaysia, D.L. Nickrent 4008 (SIU), DLN 4008, EU544343, EU544395, –, –, EU544451, –, –. Scurrula
parasitica L.: Malaysia, D.L. Nickrent 4004 (SIU), DLN 4004, EU544345, EU544397, –, –, EU544453, –, –. Scurrula pulverulenta (Wall.) G.Don: Nepal, M.
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Su & al. • Phylogenetic relationships of Santalales
TAXON 64 (3) • June 2015: 491–506
Appendix 1. Continued.
Devkota 661 (KATH), DLN 4159, EU544344, EU544396, –, –, EU544452, –, –. Socratina bemarivensis (Lecomte) Balle: Madagascar, C.C.H. Jongkind & al.
3548 (MO), DLN 4179, EU544347, EU544399, –, –, EU544454, –, –. Sogerianthe sessiliflora (S.Moore) Danser: Papua New Guinea, D.L. Nickrent & al. 4467
(WAU), DLN 4467, EU544348, EU544400, –, –, EU544455, –, –. Spirogardnera rubescens Stauffer: Australia, H.U. Stauffer & al. 5385 (Z), DLN 4546,
EF464458, –, –, EF464518, EF464497, *KP263320, –. Staufferia capuronii Z.S.Rogers, Nickrent & Malécot: Madagascar, R. Randrianaivo & al. 825 (MO),
DLN 4956, DQ329168, –, –, DQ329177, DQ329188, DQ329199, –. Strombosia grandifolia Hook.f. ex Benth.: Gabon, F.J. Breteler 15457 (WAG), DLN 4268,
DQ790123, DQ790225, –, DQ790156, DQ790192, DQ790260, –. Strombosia philippinensis S.Vidal: Philippines, D. Heuschkel, Honolulu B.G. 81.724 (SIU),
DLN 2831, AF039079, DQ790226, –, DQ790157, DQ790193, DQ790261, –. Strombosia pustulata Oliv.: Gabon, J.J. Wieringa 2781 (WAG), DLN 4054,
DQ790124, DQ790227, *KP263359, DQ790158, DQ790194, DQ790262, DQ110360. Strombosiopsis tetrandra Engl.: Gabon, J.J. Wieringa 3300 (WAG), DLN
4055, DQ790125, DQ790224, –, DQ790155, DQ790191, DQ790259, –. Struthanthus oerstedii (Oliv.) Standl.: Costa Rica, S. Sargent s.n. (SIU), DLN 2728,
L24421, EU544402, –, –, EU544457, –, –. Struthanthus woodsonii Cufod.: Costa Rica, D.L. Nickrent 2761 (SIU), DLN 2761, EU544349, EU544403, –,
EU544474, EU544458, –, –. Tapinanthus constrictiflorus (Engl.) Danser: Gabon, J.J. Wieringa 2860 (WAG), DLN 3088, (L24422), EU544404, –, –, EU544459,
–, (DQ110361). Taxillus chinensis (DC.) Danser: Malaysia, D.L. Nickrent 4032 (SIU), DLN 4032, EU544350, EU544405, –, –, EU544460, –, –. Taxillus
pseudochinensis (Yamam.) Danser: Taiwan, H.-J. Su 018 (TAI), Su 018, *KP263288, –, *KP263360, –, –, –, –. Tetrastylidium peruvianum Sleumer: Peru,
H. van der Werff & R. Vasquez 13875 (MO), DLN 4205, DQ790126, –, –, DQ790154, DQ790190, *KP263321, –. Thesium chinense Turcz.: Taiwan, C.-C. Wu
0024 (TAI), Wu 033, JQ613225, *KP263259, JQ613267, –, –, –, JQ613251. Thesium fragile L.f.: South Africa, D.L. Nickrent 4102 (SIU), DLN 4102, EF584586,
–, –, EF584608, EF584632, *KP263322, –. Thesium fruticosum A.W.Hill: South Africa, K. Steiner s.n. (SIU), DLN 2845, EF584587, –, –, EF584609, EF584633,
–, –. Thesium subsucculenta (Kammer) J.C.Manning & F.Forest: Canary Islands (Spain), A. Santos Guerra s.n. (TFNC), DLN 4374, EF584576, –, –, EF584596,
EF584621, *KP263304, –. Thonningia sanguinea Vahl: Gabon; Ghana; Cameroon, G. Walters & al. 961; H.H. Schmidt & al. 1619; J.-M. Onana 2927 (MO;
K), DLN 4382; DLN 4215; Kew DNA Bank 19155, *KP263289, –, *KP263361, –, –, –, *KP263280. Tripodanthus acutifolius (Ruiz & Pav.) Tiegh.: Brazil,
Wasum & al. 7586 (MO), DLN 2969, L24424, EU544406, –, EU544475, EU544462, *KP263323, –. Tristerix corymbosus (L.) Kuijt: Chile, V. Melzheimer s.n.;
G. Amico s.n. (SIU; BCRU), DLN 4129; DLN 4572, EF464467, EF464479, –, –, EF464512, –, –. Tupeia antarctica (G.Forst.) Cham. & Schltdl.: New Zealand,
B. Molloy s.n. (SIU), DLN 2742, L24425, DQ790208, –, DQ790133, DQ790172, –, –. Urobotrya siamensis Hiepko: Thailand, Geesink & al. 7807 (B), DLN
4369, EF584588, –, –, EF584611, EF584635, –, DQ110365. Vanwykia remota (Baker & Sprague) Wiens: Tanzania, T. Fison 91/1 (MO), DLN 4331, EU544351,
EU544407, –, –, EU544463, –, –. Viscum album L.: U.S.A., P. Faber s.n. (SIU), DLN 3024, U42821, AF389275, –, L26078, JN895000, –, –. Viscum articu
latum Burm.f.: Australia; Taiwan, D.L. Nickrent 2812; H.-J. Su 020 (SIU; TAI), DLN 2812; Su 020, JQ613228, *KP263260, (JQ613265), EF464517, EF464496,
–, –. Ximenia americana L.: Bahamas, D.L. Nickrent 2601; D. Owen s.n. (ILL; TAI), DLN 2601; Su 121, L24428, DQ790220, *KP263362, GQ997898,
GQ997871, GQ997860, *KP263281. Antirrhinum majus L.: AJ236047, AY423077, AY566619, L11688, AJ429342, GQ996966, AY453102. Arabidopsis thali
ana (L.) Heynh.: X16077, X52320, Z19121, U91966, AF144378, AF05697, NC_001284. Camellia japonica L.: U42815, AY727975, AY566627, L12602, AF380074
, (KC143082), (AF421034). Cornus florida L.: X17370, AF297532, AJ556175, (L14395), (AY526237), GQ998074, (AY725883). Myrtus communis L.: (GU476479),
EU002154, AJ556164, HM850194, AY525136, (GQ870669), GU351259. Spinacia oleracea L.: L24420, HQ843464, DQ058635, NC_002202, NC_002202,
NC_002202, AY453110.
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