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Bendiksby & al. •
Lamioideae─a taxonomic update
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60 (2) • April 2011: 471–484
INTRODUCTION
In Kubitzki’s family monograph, Harley & al. (2004) di-
vided the angiosperm family Lamiaceae into seven subfamilies.
Th e sec ond lar ge st su bfami ly, Lamioidea e (includ ing Pogo ste -
monoideae), was considered to consist of 63 genera and about
1260 species. Since Harley & al. (2004), Rydingia has been
established (Scheen & Albert, 2007), Betonica has been res-
urrected from synonymy under Stachys (Scheen & al., 2010),
Phlomoides has been resurrected and Lamiophlomis Kudô,
Notochaete Benth. and Pseuderemostachys Popov. have been
subsumed into Phlomoides (Mathiesen & al., in press). Thus,
63 genera are currently included in subfamily Lamioideae.
Recently, Scheen & al. (2010) produced a first, general
phylogenetic framework for Lamioideae based on chloroplast
DNA data, which has elucidated evolutionary relationships of
many genera and clades and permitted a preliminary tribal
classification system. For example, the molecular phylogeny
presented by Scheen & al. (2010) confirmed that Lamioideae
were non-monophyletic following earlier work by Cantino &
al. (1992), but monophyletic as circumscribed by Harley & al.
(2004), i.e., including former subfamily Pogostemonoideae.
However, the exact circumscription of the subfamily within
Lamiaceae still needs to be corroborated with better sampling
in the family.
In Cantino’s (1992a,b) morphological phylogeny of La-
miaceae, the subfamily Nepetoideae was nested within Lami-
oideae, and this group in turn emerged most closely related to
Ajuga (in Ajugoideae) and the incertae sedis genera Cymaria,
Acrymia, Holocheila and Garrettia. However, according to
more recent molecular data, the two subfamilies Lamioideae
and Nepetoideae are only remotely related, and Lamioideae
are more closely related to Scutellarioideae than to Ajugoi-
deae (Wink & Kaufmann, 1996; Wagstaff & Olmstead, 1997;
Wagstaff & al., 1998). Scheen & al. (2010) included Cymaria,
which emerged as the sister group of Lamioideae, while Scu-
tellarioideae were shown to be the phylogenetic sister of the
Cymaria-Lamioideae clade. However, a molecular survey of
An updated phylogeny and classification of Lamiaceae subfamily
Lamioideae
Mika Bendiksby,1 Lisbeth Thorbek,1 Anne-Cathrine Scheen,2 Charlotte Lindqvist3 & Olof Ryding4
1 National Centre for Biosystematics, Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, 0318 Oslo, Norway
2 Museum of Archaeology, University of Stavanger, 4036 Stavanger, Norway
3 Department of Biological Sciences, University at Buffalo (SUNY), Buffalo, New York 14260, U.S.A.
4 Botanical Garden and Museum, Natural Histor y Museum of Denmark , Universit y of Copenhagen, Gothersgade 130,
1123 Copenhagen K, Denmark
Author for correspondence: Olof Ryding, OlofR@snm.ku.dk
Abstract
Lamioideae comprise the second-largest subfamily in Lamiaceae. Although considerable progress has recently been
made in Lamioideae phylogenetics, the subfamily remains one of the most poorly investigated subfamilies in Lamiaceae. Here
we present a taxonomic update of the subfamily based on earlier published data as well as 71 new DNA extracts from relevant
in- and outgroup taxa, and DNA sequence data from four chloroplast regions (matK, rps16 , trnL intron and trnL-F spacer).
The phylogenetic positions of 10 out of 13 previously unplaced small or monoty pic Asian lamioid genera and 37 additional
lamioid species have been identified, and the classification is updated accordingly. Results from parsimony and Bayesian
phylogenetic methods corroborate earlier results, but phylogenetic resolution as well as overall branch support are improved.
All newly added genera are assigned to earlier established tribes or the new tribe Paraphlomideae Bendiksby, which includes
Ajugoides, Matsumurella and Paraphlomis. Acanthoprasium is resurrected as a genus. Transfer of species is proposed to ac-
commodate the monophyly of two genera (Lamium, Otostegia), whereas ten genera remain non-monophyletic (Ballota s.st r.,
Lagopsis, Leonotis, Leonurus, Leucas, Microtoena, Phlomoides, Sideritis, Stachys, Thuspeinanta). Eriophyton and Stachyopsis
have been included in Lamieae, Hypogomphia in Stac hydeae , and Loxocalyx in Leo nu r ea e. Betonica, Colquhounia, Galeopsis,
and Roylea remai n unclassifie d at the tr ibal level. Lamium chinense and three Ea st Asian Galeobdolon species are tr an sferred
to Matsumurella. Sulaimania and four Otostegia species are transferred to Moluccella. Alajja and three Lamium species are
transferred to Eriophyton. In total, 14 new combinations are made, one at the rank of subgenus and 13 at the rank of species.
Keywords
Acanthoprasium ; classif ication; Eriophyton ; Lamiaceae; Lamioideae; Matsumurella ; molecular phylogenetics;
Moluccella ; Paraphlomideae
Supplementary Material
The Appendix is available in the free Electronic Supplement to the online version of this article
(http://www.ingentaconnect.com/content/iapt/t ax).
Molecular Phylogenetics and BiogeograPhy
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Lamioideae─a taxonomic update
the phylogenetic positions of Acrymia, Holocheila and Garret-
tia remains to be published.
Sche en & al. (2010) al so inve stiga ted phylogene tic rel ation -
ships within Lamioideae. Based on their analyses, which were
based on three plastid markers in 159 species from 50 genera,
they discerned nine tribes within Lamioideae and discussed the
non-monophyly of some genera. Although a majority of lamioid
genera was included in their survey, some important groups
were underrepresented and a number of small or monogeneric
taxa left out. For example, 16 genera remained unclassified at
the tribal level, either because they would have formed mono-
generic tribes (Betonica, Colquhounia, Eriophyton, Galeopsis,
Paraphlomis, Roylea), or because they could not be placed
due to lack of molecular data (Ajugoides, Alajja, Hypogom-
phia, Loxocalyx, Matsumurella, Metastachydium, Paralamium,
Pseudomarrubium, Stachyopsis, Sulaimania). Three genera
were classified to tribal level, either based on morphology alone
(Colebrookea) or on morphology and limited, unpublished trnL
intron sequence data (Eurysolen, Lagopsis).
Although considerable progress has recently been made
in Lamioideae phylogenetics, the subfamily remains one of
the most poorly investigated subfamilies in Lamiaceae. For
example, only limited groups within Lamioideae have been
subjected to phylogenetic studies: e.g., tribe Lamieae (Ryding
2003), tribe Leucadeae (Ryding 1998; Scheen & Albert, 2009),
the indigenous Hawaiian labiates (Lindqvist & Albert, 2002;
Lindqvist & al., 2003), tribe Phlomoideae (Ryding, 2008; Pan,
2009; Mathiesen & al., in press), Sideritis (Ba rber & al., 2000,
2002, 2007), and tribe Synandreae (Scheen & al., 2008).
The main purpose of the present study is to determine the
phylogenetic positions of lamioid genera that were omitted in
the study of Scheen & al. (2010). A modified DNA-miniprep.
an d PCR protocol (Bendik sby & al., in prep) was us ed to obt ain
amplicons from old and presumably DNA-degraded plant tis-
sues. Moreover, in order to increase phylogenetic resolution and
branch support, some additional taxa and one additional marker
(matK) were included. Among the 64 cu r r ently recogni zed gen-
era of Lamioideae, only the monotypic genera Metastachydium,
Paralamium, and Pseudomarrubium are lacking in this study.
A few taxonomic and nomenclatural changes in accordance
with the obtained results are proposed.
MATERIALs AND METHODs
Taxon sampling. —
All taxon names in the present study
follow the “World Checklist of Lamiaceae and Verbenaceae”
(Govaerts & al., 2010), except for species belonging to Betonica
and Phlomoides, for which the Checklist is not yet updated (see
Scheen & al., 2010; Mathiesen & al., in press). Author names for
taxa included in the present study are assembled in the Appendix
(Electronic Supplement).
A total of 402 DNA sequences were generated from speci-
mens held at the following herbaria: A, BHO, C, E, GH, L, NY,
O, S, TEX, UPS, US, and WU or, in a few cases, from silica-
dried leaves (vouchers held at O). A total of 238 accessions
representing 208 species from 60 Lamioideae genera (all but
th r ee) were included as in-g roup, of which 164 acce ssions were
also used by Scheen & al. (2010). Ten genera were included
in the molecular phylogeny of subfamily Lamioideae for the
first time: Ajugoides, Alajja, Colebrookea, Eurysolen, Hypo-
gomphia, Lagopsis, Loxocalyx, Matsumurella, Stachyopsis and
Sulaimania. Colebrookea, Eurysolen and Lagopsis were in-
cluded in ord er to conf i r m the ir su ggest ed tribal position base d
on morphology or restricted and unpublished molecular data
(see Sc heen & al ., 2010). Add ition al sa mples relev ant for mono-
phyly assessments and taxonomic circumscriptions were also
included: (1) accessions of some monotypic genera or genera
re pre sente d by only a single species in Sche en & al. (2010) (e.g.,
Alajja, Colebrookea, Eurysolen, Garrettia, Lagopsis, Loxo-
calyx, Microtoena, Stachyopsis, Synandra, and Roylea); (2)
species from un-sampled geographic areas belonging to genera
with disjunct distributions (e.g., Achyrospermum wallichianum
and Pogostemon aquaticus); and (3) species that, based on mor-
phology, were expected to be extraneous to their genera (e.g.,
Ballota frutescens, Lamium chinense, L. tuberosum, Otostegia
bucharica and O. olgae).
The outgroup comprised 42 accessions, of which 18 were
extracted for the present study, including seven taxa from sub-
family Nepetoideae, five taxa from subfamily Prostantheroi-
deae, five taxa from subfamily Scutellarioideae, one taxon from
subfamily Symphorematoideae, five taxa from subfamily Aju-
goideae, five taxa from subfamily Viticoideae, and six taxa that
have not been ascribed to a subfamily (Acrymia ajugiflora,
Callicarpa americana, C. japonica, Cymaria dichotoma, Gar-
rettia siamensis, Tectona grandis ; referred to as incertae sedis
in Harley & al., 20 0 4). Finally, five me mbe rs of relat ed fa mil ies
were included as a more distant outgroup.
DNA sequence data of the trnL-F region (trnL intron and
trnL-trnF intergenic spacer) and the rps16 intron from all but
th r ee ac ces sions used by Sche en & al. (2010) were also included
in the present study, and DNA sequence data of an additional
genetic marker (matK) were generated for the same accessions,
except for about 20 DNA extracts that were no longer available.
Attempts were made to amplify and sequence all four chloro-
plast regions from 71 new DNA extracts in order to provide a
near complete generic representation of Lamioideae, a more
balanced outgroup for the phylogenetic analyses, and a bet-
ter resolved phylogeny. Sequences that were not new to this
study have been retrieved from GenBank and were originally
published by Wallander & Albert (2000), Barber & al. (2002),
Beardsley & Olmstead (2002), Bremer & al. (2002), Lindqvist
& Albert (2002), Shi & al. (2003), Paton & al. (2004), Scheen &
al. (2008), Yuan & Olmstead (2008), Scheen & Albert (2009),
Scheen & al. (2010) and Mathiesen & al. (in press). Voucher
information and GenBank accession numbers are provided in
the Appendix.
DNA extraction, PCR amplification and DNA sequencing.
—
Between 10 and 30 mg of dried plant material was crushed
twice in a 2 ml plast ic tu be with two tungst en ca rbide bead s for
1 minute at 30 Hz on a mixer mill (MM301, Retsch GmbH &
Co., Haan, Germany). Total DNA from the crushed samples was
extracted using the E.N.Z.A SP Plant DNA Mini Kit (Omega
Bio-Tek Inc., Norcross, Georgia, U.S.A.) according to the
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manufacturer’s manual. All four chloroplast regions (trnL in-
tron, trnL-trnF intergenic spacer, rp s16 intron, matK ge ne) we re
amplified and sequenced as described by Scheen & al. (2010)
unless otherwise specified. Amplification of shorter fragments
was attempted when long fragments did not amplify success-
fully, presumably due to low-quality template. For amplifica-
tion of matK we used the following six primers that were devel-
oped from available Lamiaceae matK sequences in GenBan k:
mat K-1Fa (5′-CAGGAGTATAT TTATGCATTTGC TC -3′),
matK-1Fb (5′-CTATATCCACTTATCTTTCAG GAGT-3′),
matK-3F (5′-CATGTGGAAATCTTGGTTCAAATC-3′),
matK-5Ra (5′-CAAGAAAGTCGAAGTATATACTTTA-3′),
matK-5Rb (5′-TCGAAGTATATACTTTATTCGATAC-3′),
and matK-3R (5′-TAATAAATGCAAGGAGGAAGCATC-3′).
matK was amplified either as one fragment using the primer
combination matK-1Fb and matK-5Ra, or as two shorter frag-
ments using matK-1Fb or matK-1Fa and matK-3R (the 5′ end),
and matK-3F and matK-5Ra or matK-5Rb (the 3′ end). Like-
wise, rps16 was amplified either as one fragment using the
primer combination rpsF and rpsR2R (Oxelman & al., 1997),
or as two shorter fragments using r psF or r ps-LamF and r ps-
LamR2 (the 5′ end), and rps-LamF2 and rpsR2R or rps-LamR
(the 3′ end). The following four primers were developed for
the present study from obtained Lamioideae rp s16 sequences:
rps-LamF (5′-GAARGACACGATCCGTTGTGGA-3′), rps-
LamF2 (5′-GAAGTAATGTCTAAACCCAATG-3′), rps-LamR
(5′-CGATTCGATAGATGGCTCAT TG -3′), and r ps-LamR2
(5′-ATCATTGGGTTTAGACATTACT-3′). The PCR-enzyme
AmpliTaqGold DNA Polymerase (Applied Biosystems, Fos-
ter City, California, U.S.A.) was used for amplifying DNA
obtained from old herbarium specimens or DNA extracts of
reduced quality, whereas AmpliTaq DNA Polymerase (Ap-
plied Biosystems) was used for all high-quality DNA extracts.
Samples from which amplicons were not obtained using regular
DNA miniprep- and PCR procedures, were re-assessed using
a “replicate” procedure as described by Bendiksby & al. (in
prep.). Regularly obtained PCR products were purified using
2 µl of a 1-in-10 dilution of ExoSAP-IT (enzyme/buffer stock;
USB Corporation, Cleveland, Ohio, U.S.A.) to 8 µl PCR prod-
uct, incubated at 37°C for 45 minutes followed by 15 minutes at
80°C. See Bendiksby & al. (in prep.) for purification procedure
of the “replicate” reactions. Cycle sequencing was performed
by the CEES ABI-laboratory (http://www.bio.uio.no/ABI-lab/)
using the ABI BigDye Terminator sequencing buffer and v3.1
Cycle Sequencing kit. Sequences were processed on an ABI
3730 DNA analyser (Applied Biosystems) and assembled and
edited using SEQUENCHER v.4.1.4 (Gene Codes Corporation,
Ann Arbor, Michigan, U.S.A.).
All DNA extracts generated in the present study, as well
as most of the DNA extracts included in Scheen & al. (2010),
have been deposited in the DNA/tissue collection at Natural
History Museum, Oslo (O). All sequences new to the present
study have been deposited in GenBank and accession numbers
are listed in the Appendix.
Alignment and phylogeny reconstructions. — Sequences
from 280 accessions were aligned manually using BioEdit
v.7.0.9.0 (Hall, 1999). Insertions/deletions (indels) were coded
as present/absent and added to the matrices as additional, un-
ordered characters using the program SeqState (Müller, 2005)
following the simple indel coding of Simmons & Ochoterena
(2000). The risk of DNA and/or PCR contamination increases
when usin g old and deg raded DNA. Ther efore, pa rsi mony anal-
yses of the separate regions were conducted (as described be-
low) in order to detect potential errors during the process from
leaf tissue to aligned sequence. Six contaminated sequences
were identified and excluded from further analyses, and con-
gruence of the resultant four gene-trees was confirmed prior
to concatenation. Thus, testing for contamination was done
in several ways: by separate gene tree analyses, by including
multiple accessions of taxa, and by evaluating phylogenetic
position against expectations from morphology.
Optimal models of nucleotide substitution for the vari-
ous markers were estimated using the Akaike information
criterion (AIC) and the software MrModeltest (Nylander,
2004) at the Bioportal (www.bioportal.uio.no). A partitioned
concatenated alignment of four genetic regions and 280 ac-
cessions was analyzed twice, with and without indels coded,
using MrBayes v.3.1.2 (Ronquist & Huelsenbeck, 2003) at the
Bioportal. Because long stretches of missing characters may
confound phylogenetic results in different ways, phylogenetic
analyses with and without indels coded were performed also on
a “non-orphan” matrix, i.e., including only the 259 accessions
for which at least three genetic markers were available. Poste-
rior probabilities were determined twice by r unning one cold
and four heated chains for six million generations in parallel
mode, saving trees every 1000th generation. To test whether the
Markov Chain converged, we monitored the standard deviation
of split frequencies (SDSF), which did fall below 0.01 (in all
analyses) when comparing two independent runs. The genera-
tions prior to the point when the SDSF permanently fell below
0.01 were discarded as burn-in . A 50% major ity rule co nse nsu s
tree was used to calculate posterior probabilities.
Parsimony analyses and branch support obtained from
parsimony jackknifing (Farris & al., 1996) were run using the
freely available software TNT (Goloboff & al., 2003) as de-
scribed by Scheen & al. (2010).
Alignment and phylogeny from the present study are avail-
able as Supplementary Data
to the online version of this
article (http://www.ingentaconnect.com/content/iapt/tax)
.
REsU LT s
Lengths in basepairs (bp) of the aligned DNA-regions
were: 1278 bp for the trnL-F region, 1293 bp for the rps16
intron, and 1185 bp for matK. The concatenated alignment of
the four genetic regions was 3756 bp long, and simple indel
coding recognized 526 indels. The General Time Reversible
model of nucleotide substitution with gamma distribution and
sites invariant (GTR + G + I) was the estimated best-fit model
for all genetic regions except matK, for which a simpler model
GTR + G was selected. All phylogenies obtained from Bayesian
and parsimony analyses of the full (280 accessions) and the
non-orphan (259 accessions) datasets, with and without indel
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co ding, were con gr uent, but resolved to dif ferent ext ents. Indel
coding increased overall branch support. The resolution present
in the parsimony results, with or without indel coding, was also
present in the Bayesian results. Overall, the Bayesian tree was
better resolved. The phylogenetic result from the indel-coded
Bayesian analysis of the full dataset is presented in Fig. 1, with
ranges of pa rsimony jack k nife supp or t (J K) indicated. The to-
pology was generally strongly supported, and removal of acces-
sions with long stretches of missing data resulted in increased
JK for branches of the clades concerned (Fig. 1). The number
of most-parsimonious trees was reduced drastically when or-
phans were excluded from the matrix, as was computational
time, for both the Bayesian and the parsimony analyses. The
consistency- and retention indices were highly similar in all
parsimony analyses (CI = 55–56 and RI = 86–87).
Subfamily Lamioideae formed a clade including the ten
genera that were new to this study: Alajja, Ajugoides, Cole-
brookea, Eurysolen, Hypogomphia, Lagopsis, Loxocalyx, Mat-
sumurella, Stachyopsis, and Sulaimania (Fig. 1). Colebrookea
and Eurysolen both grouped with other species of Pogoste-
moneae, Colebrookea as sister to a clade of Craniotome, Mi-
crotoena, Anisomeles, and Pogostemon, and Eurysolen as sister
a clade of Leucosceptrum, Rostrinucula and Comanthosphace
(Fig. 1A: clades a and b, respectively). Hypogomphia was
nested within Stachydeae, as sister to Thuspeinanta brahuica
(Fig. 1B). Both Ajugoides and Matsumurella formed a clade
with species of Paraphlomis and Lamium chinense (Fig. 1C).
Lagopsis and Loxocalyx were both nested within Leonureae
(Fig. 1C). Sulaimania and two species of Otostegia were ne ste d
within Moluccella (Fig. 1C). Alajja and Stachyopsis grouped
with Eriophyton and two specimens of Lamium tuberosum
(Fig. 1C).
Some genera were resolved as monophyletic with the inclu-
sion of more accessions, e.g., Gomphostemma, Melittis and Ro-
ylea (Fig. 1). However, several genera were non-monophyletic,
including Ballota, Lagopsis, Lamium, Leonotis, Leonurus, Leu-
cas, Microtoena, Moluccella, Otostegia, Phlomoides, Sideritis,
Stachys, and Thuspeinanta (Fig. 1B–C).
Acrymia and Cymaria formed a supported clade that was
sist er to the La m ioideae cla de (Fig. 1A). Subfa mily Scutella rioi-
deae was the sister of the Acrymia-Cymaria-Lamioideae clade
and Garrettia was the sister of the Scutellarioideae-Acrymia-
Cymaria-Lamioideae clade (Fig. 1A). Subfamily Viticoideae
did not form a monophyletic group (Fig. 1A).
DIsCUssION
Our expanded molecular phylogeny of subfamily Lam ioi-
deae (Fig. 1) largely corroborates the results and the taxonomic
changes proposed by Scheen & al. (2010) and Scheen & Albert
(2007). Phylogenetic affinity and tribal position have been de-
termined for the ten Lamioideae genera that were omitted in
Sche en & al. (2010; Alajja, Ajugoides, Colebrookea, Eurysolen,
Hypogomphia, Lagopsis, Loxocalyx, Matsumurella, Stachyop-
sis, Sulaimania) as well as Eriophyton and Paraphlomis, which
were previously not assigned to tribal level (see below; Fig. 1).
However, four genera remain unplaced in the updated tribal
classification of subfamily Lamioideae: Betonica, Colquhou-
nia, Galeopsis, and Roylea.
Seven genera were shown to be para- or polyphyletic by
Sche en & al. (2010): Ballota, Leonotis, Leonurus, Leucas, Phlo-
mis, Sideritis, and Stachys. Taxonomic changes proposed by
Mathiesen & al. (in press), which have been followed herein,
render Phlomis monophyletic, but the remaining six genera are
st ill para- or poly phyletic (Fig. 1B– C ). Furth ermore, our resu lts
show that non-monophyly also applies to Otostegia, Lagopsis,
Lamium, Microtoena, Moluccella, Phlomoides, and Thuspein-
anta, as currently ci rcu m scr ibe d (i.e., by Gova erts & al., 2010).
The inclusion of more data has provided increased phylogenetic
resolution and stronger support for most of the clades within
Lamioideae. For example, the clade that includes Roylea and
the three tribes Marrubieae, Lamieae and Leucadeae receives
considerably improved support (Fig. 1C). However, the phylo-
genetic position of Colquhounia receives less support in the
present study (Fig. 1B) as compared to Scheen & al. (2010).
Since most major clades were thoroughly discussed by Scheen
& al. (2010), only new results will be discussed below.
Updates on tribe Pogostemoneae. —
The new molecular
results confirm that two Asian monotypic genera, Colebrookea
and Eurysolen, belong in tribe Pogostemoneae (Fig. 1A), a
relationship previously suggested based on morphology and
limited unpublishe d DNA-se quence data (Scheen & al., 2010).
The very distinctive monotypic genus Colebrookea is re solved
as the phylogenetic sister to the large subclade of Craniotome,
Microtoena, Anisomeles and Pogostemon (Fig. 1A, clade a).
This relationship receives a posterior probability of 0.99, but
is not supported by parsimony jackknifing. Some morphologi-
cal traits of Colebrookea are similar to the genera in its sister
clade, for example, small nutlets, not much longer than broad,
Fig. 1.
The 50% majority rule consensus phylogram from a partitioned Bayesian analysis of an indel-coded, concatenated matrix of 280 acces-
sions and 3756 bp from four regions of the chloroplast genome (trnL-intron, trnL-F spacer, rps16 intron, matK). T he 3565 generations prior to
the point when the SDSF permanently fell below 0.01 (0.0077 at termination) were discarded as burn-in. Ranges of parsimony jackknife support
(JK) above 50% are indicated with dots at the branches (see inset box). Only Bayesian posterior probability values (PP) of more than 0.95 are
reported (below bra nches and in bold face). Numbers in italics above branches indicate branch support obtained from parsi mony jackk nifing on
the non-orphan dataset (259 accessions) when exceeding the range reported from the full dataset (280 accessions; i.e., values that were compa-
rable bet ween the two analyses were not reported). Accessions that were omitted from the non-or phan analysis are indicated with an asterisk.
Multiple accessions of the same species are numbered according to the Appendix. Major lamioid clades are named following the suprageneric
classification proposed by Scheen & al. (2010) and updates suggested in the present study. Lowercase let ters (a–h) indicate some of the clades
discussed in the text. The phylogeny is subdivided as follows:
A,
Outgroup that includes five non-Lamiaceae taxa, Lamiaceae subfamilies and
genera incertae sedis, and the lamioid tribe Pogostemoneae. Gray shading is used to highlight currently recognized (sensu Harley & al., 2004)
subfamilies and genera incertae sedis of the outgroup.
B,
The lamioid t axa Colquhounia, Gomphostemmateae, Synandreae, Galeopsis, Betonica
and Stachydeae.
C,
The lamioid taxa Paraphlomideae, Phlomideae, Leonureae, Roylea, Marrubieae, Lamieae and Leucadeae.
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incertae sedis
incertae sedis
incertae sedis
incertae sedis
≥
≥
≥
Ajugoideae
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≥
≥
≥
Stachydeae
C
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≥
≥
≥
Leucadeae
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with a very di stinctive scler enchy ma region, and la ck of gla nds ,
althoug h the condit ion of havi ng egla ndu lar hairs on the nut le ts
agrees better with genera in clade b.
Eurysolen is nested within the strongly supported clade
of Leucosceptrum, Rostrinucula, Comanthosphace and Achy-
rospermum (Fig. 1A: clade b). It also shares morphological
characteristics with the genera in this clade, i.e., matt and
glandular nutlets, while the other main clade within Pogoste-
moneae (clade a) has glossy and glabrous nutlets. According to
Ryding (1995), Eurysolen and most other lamioid taxa have a
sclerenchyma region in the pericarp, while the schlerenchyma
region is lacking in the other four genera of clade b. However,
whereas the sclerenchyma forms a very distinct region in most
other lamioids, it is barely distinct in Eurysolen. Hence, this
clade (clade b) is supported by having the sclerenchyma region
obsolete, indistinct or absent.
Inclusion of the African Pogostemon aquaticus and the
Asian Achyrospermum wallichianum supports the respective
monophyly of these two genera across disjunct distributions.
Pogostemon aquaticus has whorled leaves and forms a well-
supported clade with two Asian species with whorled leaves,
while the other species have opposite leaves. The phylogenetic
position of Achyrospermum wallichianum is unresolved with
respect to its African relatives.
The monotypic Asian genus Paralamium was not included
in the cu r r ent molecula r phylogeny but pre sence of sm all glossy
nutlets suggests that Paralamium belongs in clade a (Fig. 1A).
However, until this relationship is tested using molecular data
we list Paralamium as incertae sedis.
Support for two Galeopsis subgenera. —
The very dis-
tinctive genus Galeopsis, which is represented by nine acces-
sions from eight of nine currently recognized species, forms
a strongly supported clade (Fig. 1B). Its two subgenera, Gale-
opsis Rchb. and Ladanum Rchb., form two strongly supported
clades (Fig. 1B: clades c and d, respectively).
Phylogenetic affinity and tribal position of Hypogom-
phia. —
The Central Asian genus Hypogomphia was listed as
incertae sedis in the previous taxonomic treatment of subfamily
Lamioideae (Scheen & al., 2010). In the current molecular phy-
logeny, Hypogomphia is nested within tribe Stachydeae and is
strongly supported as the sister of Thuspeinanta brahuica (Fig.
1B). The genus resembles Thuspeinanta in being an nua l, havi ng
narrow leaves, 1–2-flowered cymes, and narrow oblong nutlets.
The morphology of the genus does not conf lict with the vague
description of tribe Stachydeae in Scheen & al. (2010). Hence,
Hypogomphia is included in Stachydeae. The two species of
Thuspeinanta in clud ed in the pres ent study do not group; T. pe r-
sica forms a strongly supported clade with Chamaesphacos ilici-
folius (Fig. 1B), ren der i ng Thuspeinanta para phyletic. Add it ion al
sampling of taxa within this Chamaesphacos-Hypogomphia-
Thuspeinanta clade is needed to clarify generic delimitations.
A new tribe, Paraphlomideae Bendiksby. —
The E Asian
incertae sedis and monotypic genera Matsumurella and Aju-
goides as well as one Lamium species, L. chinense, form a
clade together with Paraphlomis (Fig. 1C). Although Ajugoides,
Matsumurella, Paraphlomis, and L. chinense are morphologi-
cally similar, it has not been possible to find morphological
synapomorphies that support the whole group. Most of the
shared morphological characteristics seem to constitute ple-
siomorphic character states. However, the group can be distin-
guished from the rest of Lamioideae by possessing a combina-
tion of features as mentioned in the description (see Taxonomic
conclusions). In spite of the absence of mor phologica l sy napo-
morphies, we believe that the group deserves to be named on
the account of support from the molecular data (Fig. 1C). A
formal description of the new tribe Paraphlomideae is therefore
given below (see Taxonomic conclusions).
Within Paraphlomideae, Matsumurella tuberifera a nd two
accessions of Lamium chinense form a supported group (the
Matsumurella group; Fig. 1C), a relationship not only supported
by mor phology but also reflected in the taxonomic history.
Makino (1915) described the genus Matsumurella with only one
species, the E Asian M. tuberifera, but Ohw i (1965) and Mu rat a
& Yamazaki (1993) included it in Lamium. Wu & al. (1965)
included both M. tuberifera and L. chinense in Galeobdolon,
and described three new Chinese species G. kwangtungense,
G. szechuanense and G. yangsoense. Their generic delimitation
is followed in Chinese Floras, including Li & Hedge (1994).
In his monograph, Mennema (1989) included the European
and W Asian type species of Lamiastrum (syn. Galeobdolon)
in Lamium, but omitted or excluded Wu & al.’s (1965) five E
Asian Galeobdolon species. Ryding (in Harley & al., 2004)
resurrected Matsumurella and suggested that all the E Asian
Galeobdolon species may belong to this genus.
The E Asian Galeobdolon sp ecies are very si mil ar to each
other and there is no reason to question that the five species
belong in the same genus. However, this group is obviously
extraneous to Lamium and Lamiastrum. It differs morphologi-
cally in having the lateral corolla lobes prominent and rounded
versus triangular-acute or short and toothed in Lamium and
Lamiastrum. In our molecular tree, the representatives of the
Matsumurella group (Lamium chinense and Matsumurella tu-
berifera; Fig. 1C) do not group with the other species of La-
mium (incl. Lamiastrum, here represented by L. galeobdolon),
but group with Paraphlomis and Ajugoides. The Matsumurella
group resembles Paraphlomis, but can be distinguished from
th is ge nus in having the caly x lobes ove r hal f as long as the tube
versus less than half as long in Paraphlomis. The Matsumurella
group is morphologically less distinct from the monotypic Japa-
nese Ajugoides, with which it only groups in the non-orphan
an alysis and the n only wit h low su ppo rt (J K = 58%; not shown).
Because Matsumurella and Ajugoides together do not form
a well-supported monophyletic group in our molecular tree
(Fig. 1C), we hesitate to amalgamate the two genera into one.
Hence, we transfer the five E Asian species of Galeobdolon (or
Lamium) to the genus Matsumurella (see Taxonomic conclu-
sions). Since the two names Matsumurella and Ajugoides h ave
equal priority, the genus Matsumurella may retain its name
also if Ajugoides should be included based on a future study.
Notes on tribe Phlomideae. —
Both the phylogeny pre-
sented by Scheen & al. (2010) and the current phylogenetic
update (Fig. 1) support the split of Phlomis s.l. into two gen-
era, Phlomis s.st r. and the resu rrected Phlomoides, as recently
suggested by Mathiesen & al. (in press). That study showed
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Eremostachys, Lamiophlomis (sometimes recognized as Phlo-
mis rotata), Notochaete hamosa and Pseuderemostachys to be
nested within Phlomoides and consequently Lamiophlomis,
Pseuderemostachys and the included species of Notochaete
were transferred to Phlomoides (Mathiesen & al., in press).
In our analyses, Eremostachys is represented by f ive species
belong ing to thre e sec tions (Phlomoides Bunge, Eremostachys
and Moluccelloides Bunge), that together form a monophyletic
group within Phlomoides (Fig. 1C). The fact that E. sogdiana
(in E. sect. Eremostachys) and E. moluccelloides (in E. sect.
Moluccelloides) form a subclade of this clade supports Ryd-
ing’s (2008) suggestion that the two sections are closely related.
However, we concur with Math iesen & al. (in pr ess) that a mor e
complete survey of Eremostachys is needed.
Updates on tribe Leonureae: inclusion of Loxocalyx and
paraphyletic Lagopsis. —
The previously unplaced genus
Loxocalyx is nested within a strongly supported tribe Leon-
ureae (Fig. 1C). The two included species of Loxocalyx form a
group (JK = 62% in the non-orphan analysis) with unresolved
relationship to Lagopsis, Leonurus and Panzerina. The mor-
phology of the genus does not provide much support to the
molecular phylogeny, but hardly conflicts with it either. The
calyces of Loxocalyx slightly resemble the calyces of many
Leonureae in being zygomorphic with the abaxial lobes longer.
However, the genus lacks the apparently apomorphic features
that characterize many members of the tribe: the more or less
palmate leaf venation, and the condition of having the stamens
short or included in the corolla tube. Loxocalyx is he re in clud ed
in Leonureae on the basis of its molecular characters.
The placement of Lagopsis in Leonureae is confirmed by
adding an additional species and more DNA sequence data.
However, the two species included do not group: Lagopsis mar-
rubiastrum groups with two accessions of Panzerina lanata
whereas Lagopsis supina groups with five Leonurus species
(Fig. 1C). Thus, both Lagopsis and Leonurus ap pea r to be poly-,
or at the best, paraphyletic. The non-monophyly of Lagop-
sis and Leonurus is retained and supported in all analyses.
Clades within the Chaiturus-Lagopsis-Leonurus-Loxocalyx-
Panzerina-group do not seem to be supported by differences in
morphological characters, and the group as a whole, although
morphologically rather homogeneous, does not receive strong
support from molecular data. Because of this, we hesitate to
propose changes in the classification.
Resurrection of the genus Acanthoprasium and para-
phyly of Ballota s.str. —
The genus Ballota is polyphyletic as
cu r rently cir cumscribed (Fig. 1C) (Schee n & al., 2010). Ballota
frutescens and B. integrifolia form a clade separate from the
remaining species of Ballota (Fig. 1C). The two species differ
from other species of Ballota in having a woody habit and spiny
bracteoles versus an herbaceous habit and herbaceous bracte-
oles, and are therefore recognized as B. sect. Acanthoprasium.
The two species also differ from most other Ballota in lack-
ing branched hairs and having the calyces internally glabrous.
Sche en & al. (2010) suggest ed th at th e B. sect. Acanthoprasium
should be placed in a separate genus, but hesitated to propose
this taxonomic change as the European Ballota frutescens
was not included in their analysis. However, in our expanded
phylogeny, both species of B. sect. Acanthoprasium are in-
cluded and form a supported clade sister to all other taxa within
tribe Marrubieae (Fig. 1C). Hence, we find it appropriate at this
point to resurrect Acanthoprasium as a genus (see Taxonomic
conclusions). In his description of B. sect. Acanthoprasium,
Bentham (1832–1835) also included a species called B. forsska-
lii Benth., which is the type of Elbunis Raf. The latter name is
older than Acanthoprasium at the rank of genus. However, the
Yemeni type of B. forsskalii (Forssk ål 222 p.p. at C) belongs
to Leucas. As mentioned by Sebald (1978) the species should
be called L. alba (Forssk.) Sebald. Thus, the correct name of
the resurrected genus is Acanthoprasium.
An additional accession of Ballota nigra was included
in order to test the robustness of the phylogenetic position
of this species as sister to a clade consisting of Marrubium
and the remainder of Ballota s.str. (Scheen & al., 2010). The
two B. nigra accessions do group (Fig. 1C), and the species is
strongly supported as sister to Marrubium, retaining Ballota
s.str. paraphyletic with respect to Marrubium, even after the
exclusion of Acanthoprasium. Marrubium appears monophy-
letic, also with the inclusion of M. friwaldskyanum, but a more
thorough study of Ballota and Marrubium is needed to sort out
the generic delimitations.
Circumscriptions and subgeneric classifications of Moluc-
cella, Otostegia and Sulaimania. —
Sebald (1973) recognized
five sections within Otostegia: Otostegia, Isocheilos C h iov.
emend. Sebald, Holophyllon Kudr. emend. Sebald, Mucrophyl-
lon Sebald, and Chartocalyx ( R egel ) Chiov. em e nd. Ku d r jasc h e w
(1939). However, Scheen & Albert (2007, 2009) transferred the
species of the O. sect. Holophyllon and sect. Isocheilos to their
new genus Rydingia and O. aucheri in the monotypic O. sect.
Mucrophyllon to Moluccella and re-circumscribed Otostegia to
include only O. sect. Otostegia and O. sect. Chartocalyx. In our
expanded Lamioideae phylogeny, Otostegia sect. Chartocalyx
is represented by O. bucharica and O. olgae. These two species
do not group with species of O. sect. Otostegia (Fig. 1C), but
form a strongly supported clade with the monotypic Sulaima-
nia and two accessions of Moluccella aucheri (Fig. 1C: clade
e). This clade is the sister group to Moluccella s.str. (Fig. 1C:
clade f). Otostegia olgae also grouped with Moluccella in the
morphology-based cladogram presented by Ryding (1998).
The entire Moluccella clade (Fig. 1C: clade g) is strongly
supporte d in the molecu lar phylogeny pre sente d here. The cla de
is also supported by morphological characters, also when other
species of O. sect. Chartocalyx are included. The group can be
defined by having the nutlets apically truncate, the upper lip of
the corolla hardly bearded at the margin (although sometimes
stated to be bearded), and the calyx zygomorphic, more or less
expanded at the mouth, internally glabrous, and usually lobed
with both primary and secondary lobes. There are considerable
differences between the species, but these differences do not
seem to be as strong as suggested by other authors (Hedge &
Lamond, 1968; Sebald, 1973; Rechinger, 1982; Hedge, 1990).
Since the bracteoles are mostly smaller and softer in O. sect.
Chartocalyx than in Moluccella and Sulaimania, the plants of
this section are often considered as non-spiny, but this differ-
ence is small and hardly consistent. The calyces of Sulaimania
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otostegioides diverge in being smaller and less expanded at the
mout h, but th ey are ot her w ise not ver y dif fer ent from the cal yc es
of Moluccella and O. sect. Chartocalyx. Moreover, as mentioned
by Prain (1890) they resemble the calyces of M. spinosa in shape.
Althoug h dif fer enc es in bracts and ca lyces hardly offer good
diagnostic characters within the Moluccella gro up (Fig. 1C: cla de
g), its members can be divided into two distinctive subgroups on
the basis of differences in habit and leaf shape. One subgroup
(Fig. 1C: clade f) corresponds to Moluccella s.str., and consists
of annual or short-lived herbs with toothed or incised leaves.
The other subgroup (Fig. 1C: clade e) consists of shrublets with
the leaves entire and coriaceous to slightly fleshy, and contains
M. aucheri, O. bucharica, O. olgae and Sulaimania as well as
the rest of O. sect. Chartocalyx. Monophyly of both the larger
group (clade g) and its subgroups (clades e and f) is supported
by both molecular and morphological dat a and may deser ve the
rank of genus. We prefer, with some hesitation, to treat the large
group as a genus and the two subgroups as subgenera. Hence,
the four species of Otostegia sect. Chartocalyx and Sulaimania
otostegioides are transfer red to Moluccella, and all five species
as well as M. aucheri are included in Moluccella subg. Char-
tocalyx (clade e), while the remaining two species are included
in M. subg. Moluccella (clade f) (see Taxonomic conclusions).
The exclusion of the divergent section Chartocalyx ren-
ders Otostegia monophyletic and much more morphologically
homogeneous, and reduces its geographical distribution to a
smaller and less fragmented area. Although the transfer of this
section to Moluccella increases the variation and distribution
area of Moluccella, it is only to a moderate extent.
Generic delimitation and classification of Alajja, Eriophy-
ton, and Stachyopsis. —
In the present study, duplicate acces-
sions of three Central Asian taxa, Alajja rhomboidea, Stachy-
opsis oblongata and Lamium tuberosum, form a well-supp orted
group together with the Himalayan monotypic genus Eriophyton
(Fig. 1C). This group is sister to a strongly supported group of La-
mium in the majority rule consen sus tre e (Fig. 1C), but the sister
relationship is poorly supported. Lamium tuberosum, L. stain-
tonii, L. nepalense, and L. rhomboideum (syn. Alajja rhomboi-
deum) differ from the other species of Lamium in lacking the
characteristic short and dentate lateral lobes of the corolla. In
his monograph of Lamium, Mennema (1989) excluded these four
species from Lamium. Unfortunately, L. staintonii and L. nepal-
ense cou ld not be include d in th e prese nt st udy, but sim ila r it ies in
morphological characters suggest that all four deviating Lamium
species are related to each other and to Eriophyton and Stachyop-
sis. All members of the group except for Lamium tuberosum and
some Stachyopsis have anthers hair y with eglandular hairs, and
their hairs differ from the anther hairs in Lamium s.str. in being
shorter and not concentrated to the apices of the thecae. Lack
of parsimony jackknife support for the group consisting of Eri-
ophyton, Alajja and Lamium tuberosum (the Eriophyton group;
Fig. 1C: clade h) is likely due to large stretches of missing data
in the two accessions of L. tuberosum because strong support is
obtained for the remaining taxa when these are excluded. More-
over, the species of the Eriophyton group (clade h) all have par-
ticularly large corollas (20–40 mm long) and a corolla tube that
is much longer than the calyx. Eriophyton, Alajja, L. tuberosum
and L. staintonii all lack an annulus in the corolla tube. And, as
mentioned by Ryding (2003), L. tuberosum resembles Alajja in
having the lateral corolla lobes emarginate, but this character is
not consistent in Alajja. As mentioned by Hedge (1963), these two
species also share a “scree habit”. They have woody roots, and
thin rhizomes/stolons with the leaves scale-like at their base and
mostly congested at their apex. Eriophyton has a similar habit
but grows in a different habitat. Eriophyton and some species of
Stachyopsis have a lanate indumentum, and Alajja has a simila r
but shorter indumentum. Hedge (1990) regarded the morphologi-
cal similarities between Eriophyton and Alajja as superficial, but
as the two taxa are also very similar in molecular characters,
there are strong reasons to believe that the similarities ref lect
evolutionary relationship.
Stachyopsis emerges as sister to the Eriophyton group in
our molecular phylogeny (Fig. 1C), and seems to be sufficiently
well-defined to be retained as a genus. However, classification
of the Eriophyton group (Fig. 1C: clade h) is more problematic.
It is not possible to divide the group into distinctive genera con-
sisting of more than one species, and monotypic genera should
be avoided (unless they are highly distinct), as such entities are
redundant. We prefer to include all five species in one genus,
although this group is morphologically rather heterogeneous.
The genus is named Eriophyton as this is the oldest name in
the group (see Taxonomic conclusions).
Eriophyton s.l. and Stachyopsis together are the sister
group to trib e Lam iea e (as ci rcu m scr ibe d in Sc heen & al ., 2010)
(Fig. 1C). Most species of the three genera (Eriophyton s.l.,
Lamium s.str. and Stachyopsis) have hairy anthers. Species of
Stachyopsis and Lamium s.str. al l have a very broa d and deeply
emarginated mid-lobe of the lower lip of the corolla. Based on
these morphological characteristics and the molecular data,
Eriophyton s.l. (Fig. 1C: clade h) and Stachyopsis are included
in the tribe Lamieae, which will now consist of three genera.
Notes on Lamiaceae phylogeny. —
Although Lamiaceae
molecular phylogeny was not a prime target of the present study,
a brief discussion is appropriate as the present study has uninten-
tionally become the most comprehensive molecular phylogeny
published to date in terms of a balanced taxon sample of Lamia-
ceae subfamilies as well as number of molecular markers used.
Moreover, the four genetic markers used herein all differ from
markers employed in previous molecular studies of Lamiaceae
phylogeny (Wink & Kaufmann, 1996; Wagstaff & Olmstead,
1997; Wagstaff & al., 1998). As in these studies, the subfami-
lies Ajugoideae (Teucrioideae), Lamioideae, Nepetoideae and
Scutellarioideae form strongly supported groups (Fig. 1A). Ad-
ditionally, monophyly of the Prostantheroideae taxa included
is strongly supported (Fig. 1A). Although only prostantheroid
members of tribe Westringieae could be included here, mono-
phyly of Prostantheroideae has been confirmed from molecular
data by Olmstead & al. (1998). Viticoideae are non-monophyletic
as curre ntly ci rcu msc r ibed (Ha rl ey & al., 20 04) (Fig. 1A), which
has also been demonstrated by other molecular investigations
(Wagstaff & Olmstead, 1997; Wagstaff & al., 1998; Bramley &
al., 2009). Subfamily Symphorematoideae (here represented by
Congea) is supported in all analyses as sister to a clade consist-
ing of two viticoid genera (Petitia, Vitex) (Fig. 1A), whereas the
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incertae sedis genus Tectona groups wit h a separate clade of vi-
ticoid genera (Fig. 1A). This corroborates the results of Bramley
& al. (2009), who also included a broader viticoid taxon sample
and the symphorematoid genus Sphenodesme.
Lamioideae, Cymaria and the newly included incertae
sedis genus Acr ymia form a clade that is separated from the
rest of Lamiaceae by a long and strongly supported branch
(Fig. 1A). Subfamily Scutellarioideae is strongly supported as
the phylogenetic sister of this clade. Surprisingly, the incer-
tae sedis genus Garrettia emerges as the sister of the larger
clade consisting of these four groups. Based on morphology, a
close relationship between Cymaria, Acrymia, and Garrettia
has previously been suggested (Cantino, 1992a; Harley & al.,
2004), but the above-mentioned topology strongly suggests that
only Cymaria and Acrymia may be included in Lamioideae.
However, due to great differences in morphology, inclusion of
the two genera will make the subfamily much more heteroge-
neous and diff icult to define. Whereas Lamioideae have the
ovary 4-lobed to the base, and the nutlets hardly reticulate,
the two genera resemble many Ajugoideae in having the ovary
shallowly 4-lobed, and the nutlets reticulate. Unfortunately,
the incertae sedis genus Holocheila, which is more similar to
La mioideae in ovary an d fruit cha rac ters, co uld not be include d
in our analysis. It differs from Lamioideae in having the ovary
less deeply lobed, and the upper lip of the corolla shorter, but
according to R.G. Olmstead (unpub.), it appears to be placed
inside Lamioideae as sister to Colebrookea.
Similar to earlier phylogenies of Lamiaceae (Wink &
Kaufmann, 1996; Wagstaff & Olmstead, 1997; Wagstaff &
al., 1998), the branches between Lamiaceae subfamilies out-
side of the Lamioideae-Cymaria-Acrymia-Scutellarioideae-
Garrettia clade are generally considerably shorter and weaker
supported than they are within this clade (Fig. 1A). Moreover,
inter-relationships of subfamilies, as well as the phylogenetic
position of Callicarpa, vary between analyses of the various
genetic markers (not shown). As there presumably is no recom-
bination in the chloroplast genome, this unstable result is most
likely due to saturation or wrongly induced character homol-
ogy, which is perhaps also indicated by the long branches lead-
ing to the terminals in this part of the phylogeny. We anticipate
that increased taxon sampling will greatly improve the quality
of the alignment and thereby provide a more reliable phylog-
eny among subfamilies outside of the Lamioideae-Cymaria-
Acrymia-Scutellarioideae-Garrettia clade.
TAxONOMIC CONCLUsIONs
The following taxonomic changes are proposed as a result
of our new phylogeny of Lamioideae (Fig. 1).
Lamiaceae subfam. Lamioideae tribe Paraphlomideae Ben-
di k sby, tr. nov. – Type: Paraphlomis Prain in J. Asiat. Soc.
Bengal, Pt. 2, Nat. Hist. 74: 721. 1908.
Herbae perennes, subfrutices vel forsan interdum herbae
annuae, plerumque rhizomatosae vel in parte stoloniformes.
Omnes pili non-ramosi, vix lanati. Calyces actinomorphi vel
subactinomor phi, non dilatati ad orificium, 5-lobati sed lobi
interdum brevissimi. Corollae valde 2-labiatae, 8–22 mm
longae, labium superum extra pubescens, ad marginem vix
barbatum, labium infernum 3-lobatum cum lobis prominenti-
bus rotundatis integris. Stamina tubo corollae longiora, labio
supero vix longiora, antherae glabrae vel glanduliferae cum
glandulis sessilibus. Apex nucularum truncatus, subtruncatus
vel inderdum rotundatus.
Perennial herbs, subshrubs, or perhaps sometimes annuals,
mostly rhizomatous or stoloniferous. Indumentum of unbranched
hairs only, hardly lanate. Calyces actinomorphic or almost so,
not expanded at the mouth, 5-lobed but lobes sometimes very
short. Corolla st rongly 2-lipped , 8–22 mm long, upper lip hai r y,
but hardly bearded along the margin, lower lip 3-lobed with the
lateral lobes prominent, rounded and entire. Stamens protruding
beyond the mouth of the corolla tube, but hardly longer than the
upper lip, anthers glabrous or with sessile glands. Nutlets apically
truncate, subtruncate or sometimes rounded.
Included genera: Paraphlomis Prain, Matsumurella
Makino, Ajugoides Makino.
Matsumurella Makino in Bot. Mag. (Tokyo) 29: 279. 1915
≡ Galeobdolon sect. Matsumurella (Makino) C.Y. Wu &
Hsuan in Acta Phytotax. Sin. 10: 157. 1965 – Ty p e: M. tu-
berifera (Makino) Makino.
= Galeobdolon sect. Biflora C.Y. Wu & Hsuan in Acta Phyto-
tax. Sin. 10: 159. 1965 – Type: G. kwantungense C.Y. Wu.
Ryding’s description of Matsumurella in Harley & al.
(2004) should be modified in the following respect: Perennial
herbs, subshrubs or perhaps also annual herbs. Five species in
China, Japan and Taiwan.
Matsumurella chinensis (Benth.) Bendiksby, comb. nov. ≡
Lamium chinense Benth. in Candolle, Prodr. 12: 512. 1848
≡ Galeobdolon chinense (Benth.) C.Y. Wu in Acta Phyto-
tax. Sin. 10: 157. 1965.
Matsumurella kwangtungensis (C.Y. Wu) Bendiksby, comb.
nov. ≡ Galeobdolon kwangtungense C.Y. Wu in Acta Phy-
totax. Sin. 10: 160. 1965.
Matsumurella szechuanensis (C.Y. Wu) Bendiksby, comb.
nov. ≡ Galeobdolon szechuanense C.Y. Wu in Acta Phy-
totax. Sin. 10: 159. 1965.
Matsumurella tuberifera (Makino) Makino in Bot. Mag.
(Tokyo) 29: 279. 1915 ≡ Leonurus tuberiferus Makino in
Bot. Mag. (Tokyo) 19: 146. 1905 ≡ Lamium tuberiferum
(Makino) Ohwi in J. Jap. Bot. 12: 327. 1936 ≡ Lamium
chinense Ben th. var. tuberiferum (Maki no) Mu rat a in Acta.
Phytotax. Geobot. 15: 176. 1954 ≡ Galeobdolon tuberiferum
(Makino) C.Y. Wu in Acta Phytotax. Sin. 10: 158. 1965.
= Lamium kelungense Hayata in Icon. Pl. Formosan. 8: 91. 1919.
Matsumurella yangsoensis (Y.Z. Sun) Bendiksby, comb. nov.
≡ Galeobdolon yangsoense Y.Z. Sun in Acta Phytotax.
Sin. 10: 160. 1965.
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Acanthoprasium (Bent h .) Spenn. in T. Nees, Gen. Fl. Germ.
2: [no page number]. 1843 ≡ Ballota sec t. Acanthoprasium
Benth., Labiat. Gen. Spec.: 598. 1834 – Type: A. frutescens
(L.) Spenn.
Small shrubs, with simple hairs only. Inflorescences rac-
emoid or thyrsoid, cymes 1–3-flowered, bracteoles in pairs,
prominent, spinose. Calyx broadly campanulate, lobes spiny,
5 and subequal, or 6–10 wit h the secondar y lobes smaller. Co-
rolla strongly 2-lipped, tube annulate inside, upper lip entire
or shallowly emarginate, hairy above, but not bearded with
longer hairs at the margin, lower lip 3-lobe d. Th eca e ± distin ct.
Style-lobes slightly unequal. Nutlets apically rounded, hairy or
smooth. Two species in the Maritime Alps and Cypr us.
Acanthoprasium frutescens (L.) Spenn. in T. Nees, Gen. Fl.
Germ. 2: [no page number]. 1843 ≡ Moluccella frutescens
L., Sp. Pl.: 587. 1753 ≡ Ballota spinosa Link, Handbuch
1: 475. 1829 ≡ Beringeria frutescens (L.) Rchb., Fl. Germ.
Excurs.: 325. 1831 ≡ Ballota frutescens (L.) Woods, Tour-
ist’s Fl.: 295. 1850.
Acanthoprasium integrifolium (Be nt h.) Ryd ing, comb. nov. ≡
Ballota integrifolia Benth., Labiat. Gen. Spec.: 599. 1834.
= Ballota wettsteinii Rech. in Oesterr. Bot. Z. 40: 153. 1890.
Moluccella L., Sp. Pl.: 587. 1753 – Type: M. laevis L.
After five more species are included, Ryding’s description
in Harley & al. (2004) has to be modified as follows: Perennial
shrublets, or annual or short-lived herbs. Stems and leaves
glabrescent or hairy with short hairs. Bracteoles more or less
spiny. Calyx zygomorphic, mostly also 2-lipped, tube strongly
or sometimes only slightly expanded (M. otostegioides). Eight
species from S Europe to Central Asia, Pakistan and Kashmir.
M. subg. Moluccella
Annual or short-lived perennial herbs, glabrescent, leaves
thin, almost palmately crenate, serrate or incised. Two species
from southern Europe to Central Asia.
Moluccella laevis L., Sp. Pl.: 587. 1753.
Moluccella spinosa L., Sp. Pl.: 587. 1753.
Moluccella subg. Chartocalyx (Regel) Ryding, comb. et stat.
nov. ≡ Chartocalyx Regel in Trudy Imp. S.-Peterburgsk.
Bot. Sada 6: 367. 1879, non Chartacalyx Maingay ex Ma st.
1874 ≡ Harmsiella Briq. in Engler & Pra ntl, Nat. Pf la nzen-
fam., Nachtr. 1: 291. 1897 ≡ Otostegia sect. Chartocalyx
(Regel) Chiov. in Malphigia 34: 521. 1937 – Type: M. olgae
(Regel) Ryding.
= Sulaimania Hedge & Rech. f. in Rechinger, Fl. Iranica 150:
345. 1982 – Type: S. otostegioides (Prai n) Hedge & Rec h. f.
Perennial shrublets, glabrescent or shortly hairy, leaves
entire, coriaceous to slightly fleshy. Central Asia to Pakistan
and Kashmir.
Briquet (1897) regarded Chartocalyx as a you nge r homonym
of a genus name in Tiliaceae, and proposed Harmsiella as a new
name of this labiate genus. However, the genus in Tiliaceae is
called Chartacalyx, and it is questionable whether this name is
similar enough to be regarded as a homonym of Chartocalyx.
Here, we follow Sebald (1973), Govaerts & al. (2010) and other
authors in regarding the name Chartocalyx as legitimate.
Moluccella aucheri (Boiss.) A.-C. Scheen in Syst. & Geogr.
Pl. 77: 234. 2007 ≡ Otostegia aucheri Boiss., Diagn. Pl.
Orient. 5: 40. 1844.
Moluccella bucharica (B. Fedts ch.) Ryding, comb. nov. ≡ Oto-
stegia bucharica B. Fedtsch. in Izv. Imp. Bot. Sada Petra
Velikago 15: 2. 1915.
Moluccella fedtschenkoana (Kudr.) Ryding, comb. nov. ≡
Otostegia fedtschenkoana Kudr., Fragm. K Monogr. Oto-
stegia: 28. 1939.
Moluccella olgae (Regel) Ryding, comb. nov. ≡ Chartocalyx
olgae Regel in Trudy Imp. S.-Peterburgsk. Bot. Sada 6:
368. 1879 ≡ Otostegia olgae (Regel) Korsh. in Zap. Imp.
Akad. Nauk Fiz.-Mat. Otd., ser. 8, 4(4): 96. 1896 ≡ Harm-
siella olgae (Regel) K. Schum. in Just’s Bot. Jahresber.
28(1): 484. 1902.
Moluccella otostegioides Prain in J. Asiat. Soc. Bengal, Pt. 2,
Nat. Hist. 59: 311. 1891 ≡ Sulaimania otostegioides (Pr ain)
Hedge & Rech. f. in Rechinger, Fl. Iran ica 150: 345. 1982.
Moluccella sogdiana (Kudr.) Ryd ing, comb. nov. ≡ Otostegia
sogdiana Kudr., Fragm. K Monogr. Otostegia: 24. 1939.
Eriophyton Benth. in Wallich, Pl. Asiat. Rar. 1: 63. 1830 – Type:
E. wallichii Benth.
= Erianthera Benth. in Hooker’s J. Bot. Kew Ga rd. Misc. 3: 880.
1833, nom illeg., non Nees 1832 ≡ Alajja Ikonn. in Novosti
Sist. Vyssh. Rast. 8: 274. 1971 ≡ Susilkumara Bennet, In-
dian Forester 107: 432. 1981 – Type: E. rhomboidea Benth.
After four species are included in this earlier monotypic
genus, Ryding’s description in Harley & al. (2004) has to be
modified as follows: Perennial herbs with a woody root, and
unbranched hairs. Calyx actinomorphic or almost so, sub-
equally 5-lobed. Corolla 20–40 mm long, tube much longer
than the calyx, exannulate or sometimes annulate, upper lip
hairy above, not bearded along the margin, lower lip 3-lobed,
mid-lobe slightly to much larger than the lateral lobes, emar-
ginate to almost entire, lateral lobes prominent, rounded or
em arg i nat e. Nut lets ap ic ally truncate or su btr u n cate. Five or six
species growing in alpine area at 2700–5000 m in Tadzhikistan,
Afghanistan, N Pakistan, S China, Nepal and N India.
Eriophyton nepalense (Hed ge) Ryding, comb. nov. ≡ Lamium
nepalense Hedge in Notes Roy. Bot. Gard. Edinburgh 29:
30. 1969.
Eriophyton rhomboideum ( Benth.) Ryding, comb. nov. ≡ Erian-
thera rhomboidea B e n t h . in Ho o ker’s J. Bo t . Kew Ga r d . Mi s c .
483
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rhomboidea (Bent h.) Bennet, Indian Forest er 107: 433. 1981.
= Erianthera anomala Ju z. in Bot. Mat er. Ger b. Bot . Inst. Kom-
arova Akad. Nauk S.S.S.R. 15: 269. 1953 ≡ Alajja anomala
(Juz.) Ikonn. in Novosti Sist. Vyssh. Rast. 8: 274. 1971.
= Eriophyton afghanicum Rech. f. in Biol. Skr. 8(1): 58. 1955 ≡
Alajja afghanica (Rech. f.) Ikonn. in Novosti Sist. Vyssh.
Rast. 8: 274. 1971.
Govaerts & al. (2010) and some other authors treated Alajja
anomala as a specie s, but Hedge (1990) include d it as a sy nonym
under E. rhomboideum. We tend to agree with Hedge (1990).
Eriophyton staintonii (Hedge) Ryding, comb. nov. ≡ Lamium
staintonii Hedge in Notes Roy. Bot. Gard. Edinburgh 29:
29. 1969.
Eriophyton tuberosum (Hed ge) Ryd ing, comb. nov. ≡ Lamium
tuberosum Hedge in Notes Roy. Bot. Gard. Edinbu rgh 25:
49. 1963.
= Lamium gilongense H.W. Li, Fl. Xi zangic a 4: 163. 1985 (syn.
fide Yonekura, 2008).
Eriophyton wallichii Benth. in Wallich, Pl. Asiat. Rar. 1: 63.
1830 ≡ E. wallichianum Hook. f., Fl. Brit. India 4: 694.
1885, orth. var.
Otostegia Benth., Labiat. Gen. Spec.: 601. 1834.
Af t er four of the five sec tions are excluded from th e genus ,
Budantsev’s description in Harley & al. (2004) has to be modi-
fied as follows: Bracteoles herbaceous to slightly spiny, spiny
bracteoles sometimes extending to nodes of ordinary leaves.
Calyx slightly to strongly zygomorphic, tube with an annulus
of eglandular hairs near the mouth of its narrow proximal part.
Corolla white, upper lip densely hairy and bearded with the
hairs longer at the margin than on the upper surface. Nutlets
rounded at the apex. About eight species, from NE Cameroun
to W Saudi Arabia and Yemen, and in Egypt (Sinai).
ACKNOWLEDGEMENTs
The authors thank the curators at A, BHO, E, GH, L, N Y, O, S,
TEX, UPS, US, and WU for permission to sample from herbarium
sp ec ime ns used in this study, Rich ard G. Ol mst ea d for a DNA sam ple
of Gomphostemma javanicum, Janet Barber for DNAs of Sideritis,
Philip D. Cantino for providing silica-dried material of Chelonopsis
moschata, an d Cha rl ot t e S. Bjo rå for pr ov id i ng silica -dr ied mat eri al of
Salvia nilotica and Leucas volkensii and for helping out with various
tasks. Victor A. Albert is thanked for writing the proposal for the grant
(no. 154145 fr om th e Re sea rch Cou ncil of Nor way) that has su pporte d
the present paper. Liv Borgen, Anne K. Brysting, Inger Nordal and
Marte Holten Jørgensen are thanked for valuable comments on the
manuscr ipt. Finally, we are most grateful to Richard G. Olmstead,
two anonymous rev iewers and the editor, Mar y Endr ess, for positive,
useful and rapid feedback on our submitted manuscript.
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