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Bendiksby & al. • Lamioideae─a taxonomic update
M O L E C U L A R PH Y LO G E N E T I C S A N D B I O G E O G R A PH Y
An updated phylogeny and classification of Lamiaceae subfamily
Lamioideae
Mika Bendiksby,1 Lisbeth Thorbek,1 Anne-Cathrine Scheen, 2 Charlotte Lindqvist 3 & Olof Ryding4
1
2
3
4
National Centre for Biosystematics, Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, 0318 Oslo, Norway
Museum of Archaeology, University of Stavanger, 4036 Stavanger, Norway
Department of Biological Sciences, University at Buffalo (SUNY), Buffalo, New York 14260, U.S.A.
Botanical Garden and Museum, Natural History Museum of Denmark, University 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 monotypic 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 accommodate the monophyly of two genera (Lamium, Otostegia), whereas ten genera remain non-monophyletic (Ballota s.str.,
Lagopsis, Leonotis, Leonurus, Leucas, Microtoena, Phlomoides, Sideritis, Stachys, Thuspeinanta). Eriophyton and Stachyopsis
have been included in Lamieae, Hypogomphia in Stachydeae, and Loxocalyx in Leonureae. Betonica, Colquhounia, Galeopsis,
and Roylea remain unclassified at the tribal level. Lamium chinense and three East Asian Galeobdolon species are transferred
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 ; classification; 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/tax).
INTRODUCTION
In Kubitzki’s family monograph, Harley & al. (2004) divided the angiosperm family Lamiaceae into seven subfamilies.
The second largest subfamily, Lamioideae (including Pogostemonoideae), 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 resurrected 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 Lamiaceae, the subfamily Nepetoideae was nested within Lamioideae, 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 Ajugoideae (Wink & Kaufmann, 1996; Wagstaff & Olmstead, 1997;
Wagstaff & al., 1998). Scheen & al. (2010) included Cymaria,
which emerged as the sister group of Lamioideae, while Scutellarioideae were shown to be the phylogenetic sister of the
Cymaria-Lamioideae clade. However, a molecular survey of
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the phylogenetic positions of Acrymia, Holocheila and Garrettia remains to be published.
Scheen & al. (2010) also investigated phylogenetic relationships 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 monogeneric tribes (Betonica, Colquhounia, Eriophyton, Galeopsis,
Paraphlomis, Roylea), or because they could not be placed
due to lack of molecular data (Ajugoides, Alajja, Hypogomphia, 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 (Barber & 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.
and PCR protocol (Bendiksby & al., in prep) was used to obtain
amplicons from old and presumably DNA-degraded plant tissues. Moreover, in order to increase phylogenetic resolution and
branch support, some additional taxa and one additional marker
(matK) were included. Among the 64 currently recognized genera 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 specimens 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 silicadried leaves (vouchers held at O). A total of 238 accessions
representing 208 species from 60 Lamioideae genera (all but
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three) were included as in-group, of which 164 accessions 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, Hypogomphia, Lagopsis, Loxocalyx, Matsumurella, Stachyopsis and
Sulaimania. Colebrookea, Eurysolen and Lagopsis were included in order to confirm their suggested tribal position based
on morphology or restricted and unpublished molecular data
(see Scheen & al., 2010). Additional samples relevant for monophyly assessments and taxonomic circumscriptions were also
included: (1) accessions of some monotypic genera or genera
represented by only a single species in Scheen & al. (2010) (e.g.,
Alajja, Colebrookea, Eurysolen, Garrettia, Lagopsis, Loxocalyx, 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 morphology, 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 subfamily Nepetoideae, five taxa from subfamily Prostantheroideae, five taxa from subfamily Scutellarioideae, one taxon from
subfamily Symphorematoideae, five taxa from subfamily Ajugoideae, five taxa from subfamily Viticoideae, and six taxa that
have not been ascribed to a subfamily (Acrymia ajugiflora,
Callicarpa americana, C. japonica, Cymaria dichotoma, Garrettia siamensis, Tectona grandis ; referred to as incertae sedis
in Harley & al., 2004). Finally, five members of related families
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
three accessions used by Scheen & 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 chloroplast 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 better 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 plastic tube with two tungsten carbide beads 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 intron, trnL-trnF intergenic spacer, rps16 intron, matK gene) were
amplified and sequenced as described by Scheen & al. (2010)
unless otherwise specified. Amplification of shorter fragments
was attempted when long fragments did not amplify successfully, presumably due to low-quality template. For amplification of matK we used the following six primers that were developed from available Lamiaceae matK sequences in GenBank:
matK-1Fa (5′-CAGGAGTATATTTATGCATTTGCTC-3′),
matK-1Fb (5′-CTATATCCACTTATCTTTCAGGAGT-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 fragments using matK-1Fb or matK-1Fa and matK-3R (the 5′ end),
and matK-3F and matK-5Ra or matK-5Rb (the 3′ end). Likewise, rps16 was amplified either as one fragment using the
primer combination rpsF and rpsR2R (Oxelman & al., 1997),
or as two shorter fragments using rpsF or rps-LamF and rpsLamR2 (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 rps16 sequences:
rps-LamF (5′-GAARGACACGATCCGTTGTGGA-3′), rpsLamF2 (5′-GAAGTAATGTCTAAACCCAATG-3′), rps-LamR
(5′-CGATTCGATAGATGGCTCATTG-3′), and rps-LamR2
(5′-ATCATTGGGTTTAGACATTACT-3′). The PCR-enzyme
AmpliTaqGold DNA Polymerase (Applied Biosystems, Foster 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 (Applied 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 product, 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
Bendiksby & al. • Lamioideae─a taxonomic update
as present/absent and added to the matrices as additional, unordered 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 using old and degraded DNA. Therefore, parsimony analyses of the separate regions were conducted (as described below) 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 congruence 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 various 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 accessions 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. Posterior probabilities were determined twice by running 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 generations prior to the point when the SDSF permanently fell below
0.01 were discarded as burn-in. A 50% majority rule consensus
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 described by Scheen & al. (2010).
Alignment and phylogeny from the present study are available as Supplementary Data to the online version of this
article (http://www.ingentaconnect.com/content/iapt/tax).
REsULTs
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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coding, were congruent, but resolved to different extents. 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 parsimony jackknife support (JK) indicated. The topology was generally strongly supported, and removal of accessions 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 orphans 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, Colebrookea, Eurysolen, Hypogomphia, Lagopsis, Loxocalyx, Matsumurella, Stachyopsis, and Sulaimania (Fig. 1). Colebrookea
and Eurysolen both grouped with other species of Pogostemoneae, Colebrookea as sister to a clade of Craniotome, Microtoena, 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 nested
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 inclusion of more accessions, e.g., Gomphostemma, Melittis and Roylea (Fig. 1). However, several genera were non-monophyletic,
including Ballota, Lagopsis, Lamium, Leonotis, Leonurus, Leucas, Microtoena, Moluccella, Otostegia, Phlomoides, Sideritis,
Stachys, and Thuspeinanta (Fig. 1B–C).
Acrymia and Cymaria formed a supported clade that was
sister to the Lamioideae clade (Fig. 1A). Subfamily Scutellarioideae was the sister of the Acrymia-Cymaria-Lamioideae clade
and Garrettia was the sister of the Scutellarioideae-AcrymiaCymaria-Lamioideae clade (Fig. 1A). Subfamily Viticoideae
did not form a monophyletic group (Fig. 1A).
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DIsCUssION
Our expanded molecular phylogeny of subfamily Lamioideae (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 determined for the ten Lamioideae genera that were omitted in
Scheen & al. (2010; Alajja, Ajugoides, Colebrookea, Eurysolen,
Hypogomphia, Lagopsis, Loxocalyx, Matsumurella, Stachyopsis, 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, Colquhounia, Galeopsis, and Roylea.
Seven genera were shown to be para- or polyphyletic by
Scheen & al. (2010): Ballota, Leonotis, Leonurus, Leucas, Phlomis, 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
still para- or polyphyletic (Fig. 1B–C). Furthermore, our results
show that non-monophyly also applies to Otostegia, Lagopsis,
Lamium, Microtoena, Moluccella, Phlomoides, and Thuspeinanta, as currently circumscribed (i.e., by Govaerts & 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 phylogenetic 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 unpublished DNA-sequence data (Scheen & al., 2010).
The very distinctive monotypic genus Colebrookea is resolved
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 morphological 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 accessions and 3756 bp from four regions of the chloroplast genome (trnL-intron, trnL-F spacer, rps16 intron, matK). The 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 branches and in bold face). Numbers in italics above branches indicate branch support obtained from parsimony jackknifing on
the non-orphan dataset (259 accessions) when exceeding the range reported from the full dataset (280 accessions; i.e., values that were comparable between the two analyses were not reported). Accessions that were omitted from the non-orphan 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 letters (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 taxa 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
Ajugoideae
incertae sedis
incertae sedis
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≥
≥
≥
Stachydeae
C
476
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Bendiksby & al. • Lamioideae─a taxonomic update
≥
Leucadeae
≥
≥
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Bendiksby & al. • Lamioideae─a taxonomic update
with a very distinctive sclerenchyma region, and lack of glands,
although the condition of having eglandular hairs on the nutlets
agrees better with genera in clade b.
Eurysolen is nested within the strongly supported clade
of Leucosceptrum, Rostrinucula, Comanthosphace and Achyrospermum (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 Pogostemoneae (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 wellsupported 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 current molecular phylogeny but presence of small 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 distinctive genus Galeopsis, which is represented by nine accessions from eight of nine currently recognized species, forms
a strongly supported clade (Fig. 1B). Its two subgenera, Galeopsis Rchb. and Ladanum Rchb., form two strongly supported
clades (Fig. 1B: clades c and d, respectively).
Phylogenetic affinity and tribal position of Hypogomphia. — 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 phylogeny, Hypogomphia is nested within tribe Stachydeae and is
strongly supported as the sister of Thuspeinanta brahuica (Fig.
1B). The genus resembles Thuspeinanta in being annual, having
narrow leaves, 1–2-flowered cymes, and narrow oblong nutlets.
The morphology of the genus does not conflict with the vague
description of tribe Stachydeae in Scheen & al. (2010). Hence,
Hypogomphia is included in Stachydeae. The two species of
Thuspeinanta included in the present study do not group; T. persica forms a strongly supported clade with Chamaesphacos ilicifolius (Fig. 1B), rendering Thuspeinanta paraphyletic. Additional
sampling of taxa within this Chamaesphacos-HypogomphiaThuspeinanta clade is needed to clarify generic delimitations.
A new tribe, Paraphlomideae Bendiksby. — The E Asian
incertae sedis and monotypic genera Matsumurella and Ajugoides as well as one Lamium species, L. chinense, form a
clade together with Paraphlomis (Fig. 1C). Although Ajugoides,
Matsumurella, Paraphlomis, and L. chinense are morphologically similar, it has not been possible to find morphological
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TAXON 60 (2) • April 2011: 471–484
synapomorphies that support the whole group. Most of the
shared morphological characteristics seem to constitute plesiomorphic character states. However, the group can be distinguished from the rest of Lamioideae by possessing a combination of features as mentioned in the description (see Taxonomic
conclusions). In spite of the absence of morphological synapomorphies, 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 and two
accessions of Lamium chinense form a supported group (the
Matsumurella group; Fig. 1C), a relationship not only supported
by morphology but also reflected in the taxonomic history.
Makino (1915) described the genus Matsumurella with only one
species, the E Asian M. tuberifera, but Ohwi (1965) and Murata
& 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 species are very similar 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 morphologically 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 tuberifera; Fig. 1C) do not group with the other species of Lamium (incl. Lamiastrum, here represented by L. galeobdolon),
but group with Paraphlomis and Ajugoides. The Matsumurella
group resembles Paraphlomis, but can be distinguished from
this genus in having the calyx lobes over half as long as the tube
versus less than half as long in Paraphlomis. The Matsumurella
group is morphologically less distinct from the monotypic Japanese Ajugoides, with which it only groups in the non-orphan
analysis and then only with low support (JK = 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 conclusions). Since the two names Matsumurella and Ajugoides have
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 presented by Scheen & al. (2010) and the current phylogenetic
update (Fig. 1) support the split of Phlomis s.l. into two genera, Phlomis s.str. and the resurrected Phlomoides, as recently
suggested by Mathiesen & al. (in press). That study showed
TAXON 60 (2) • April 2011: 471–484
Eremostachys, Lamiophlomis (sometimes recognized as Phlomis 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 five species
belonging to three sections (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 Ryding’s (2008) suggestion that the two sections are closely related.
However, we concur with Mathiesen & al. (in press) that a more
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 Leonureae (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 morphology 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 here included
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 marrubiastrum groups with two accessions of Panzerina lanata
whereas Lagopsis supina groups with five Leonurus species
(Fig. 1C). Thus, both Lagopsis and Leonurus appear to be poly-,
or at the best, paraphyletic. The non-monophyly of Lagopsis and Leonurus is retained and supported in all analyses.
Clades within the Chaiturus-Lagopsis-Leonurus-LoxocalyxPanzerina-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 paraphyly of Ballota s.str. — The genus Ballota is polyphyletic as
currently circumscribed (Fig. 1C) (Scheen & 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 bracteoles, and are therefore recognized as B. sect. Acanthoprasium.
The two species also differ from most other Ballota in lacking branched hairs and having the calyces internally glabrous.
Scheen & al. (2010) suggested that the 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
Bendiksby & al. • Lamioideae─a taxonomic update
phylogeny, both species of B. sect. Acanthoprasium are included 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. forsskalii 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 (Forsskål 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 monophyletic, 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 Moluccella, Otostegia and Sulaimania. — Sebald (1973) recognized
five sections within Otostegia: Otostegia, Isocheilos Chiov.
emend. Sebald, Holophyllon Kudr. emend. Sebald, Mucrophyllon Sebald, and Chartocalyx (Regel) Chiov. emend. Kudrjaschew
(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 Sulaimania 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
supported in the molecular phylogeny presented here. The clade
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 difference is small and hardly consistent. The calyces of Sulaimania
479
Bendiksby & al. • Lamioideae─a taxonomic update
otostegioides diverge in being smaller and less expanded at the
mouth, but they are otherwise not very different from the calyces
of Moluccella and O. sect. Chartocalyx. Moreover, as mentioned
by Prain (1890) they resemble the calyces of M. spinosa in shape.
Although differences in bracts and calyces hardly offer good
diagnostic characters within the Moluccella group (Fig. 1C: clade
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 data and may deserve 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 transferred to Moluccella, and all five species
as well as M. aucheri are included in Moluccella subg. Chartocalyx (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 renders 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, Eriophyton, and Stachyopsis. — In the present study, duplicate accessions of three Central Asian taxa, Alajja rhomboidea, Stachyopsis oblongata and Lamium tuberosum, form a well-supported
group together with the Himalayan monotypic genus Eriophyton
(Fig. 1C). This group is sister to a strongly supported group of Lamium in the majority rule consensus tree (Fig. 1C), but the sister
relationship is poorly supported. Lamium tuberosum, L. staintonii, L. nepalense, and L. rhomboideum (syn. Alajja rhomboideum) 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. nepalense could not be included in the present study, but similarities in
morphological characters suggest that all four deviating Lamium
species are related to each other and to Eriophyton and Stachyopsis. All members of the group except for Lamium tuberosum and
some Stachyopsis have anthers hairy 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 Eriophyton, 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. Moreover, the species of the Eriophyton group (clade h) all have particularly large corollas (20–40 mm long) and a corolla tube that
is much longer than the calyx. Eriophyton, Alajja, L. tuberosum
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TAXON 60 (2) • April 2011: 471–484
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 similar
but shorter indumentum. Hedge (1990) regarded the morphological 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 reflect
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 consisting 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 tribe Lamieae (as circumscribed in Scheen & 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. all have a very broad 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 unintentionally become the most comprehensive molecular phylogeny
published to date in terms of a balanced taxon sample of Lamiaceae 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 subfamilies Ajugoideae (Teucrioideae), Lamioideae, Nepetoideae and
Scutellarioideae form strongly supported groups (Fig. 1A). Additionally, monophyly of the Prostantheroideae taxa included
is strongly supported (Fig. 1A). Although only prostantheroid
members of tribe Westringieae could be included here, monophyly of Prostantheroideae has been confirmed from molecular
data by Olmstead & al. (1998). Viticoideae are non-monophyletic
as currently circumscribed (Harley & al., 2004) (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 consisting of two viticoid genera (Petitia, Vitex) (Fig. 1A), whereas the
TAXON 60 (2) • April 2011: 471–484
incertae sedis genus Tectona groups with a separate clade of viticoid 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 Acrymia 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 incertae 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 heterogeneous and difficult 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
Lamioideae in ovary and fruit characters, could not be included
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 outside of the Lamioideae-Cymaria-Acrymia-ScutellarioideaeGarrettia 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 recombination in the chloroplast genome, this unstable result is most
likely due to saturation or wrongly induced character homology, which is perhaps also indicated by the long branches leading 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 phylogeny among subfamilies outside of the Lamioideae-CymariaAcrymia-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 Bendiksby, 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
Bendiksby & al. • Lamioideae─a taxonomic update
subactinomorphi, 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 prominentibus 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 strongly 2-lipped, 8–22 mm long, upper lip hairy,
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 – Type: M. tuberifera (Makino) Makino.
= Galeobdolon sect. Biflora C.Y. Wu & Hsuan in Acta Phytotax. 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 Phytotax. Sin. 10: 157. 1965.
Matsumurella kwangtungensis (C.Y. Wu) Bendiksby, comb.
nov. ≡ Galeobdolon kwangtungense C.Y. Wu in Acta Phytotax. Sin. 10: 160. 1965.
Matsumurella szechuanensis (C.Y. Wu) Bendiksby, comb.
nov. ≡ Galeobdolon szechuanense C.Y. Wu in Acta Phytotax. 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 Benth. var. tuberiferum (Makino) Murata 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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Bendiksby & al. • Lamioideae─a taxonomic update
TAXON 60 (2) • April 2011: 471–484
Acanthoprasium (Benth.) Spenn. in T. Nees, Gen. Fl. Germ.
2: [no page number]. 1843 ≡ Ballota sect. Acanthoprasium
Benth., Labiat. Gen. Spec.: 598. 1834 – Type: A. frutescens
(L.) Spenn.
Small shrubs, with simple hairs only. Inflorescences racemoid or thyrsoid, cymes 1–3-flowered, bracteoles in pairs,
prominent, spinose. Calyx broadly campanulate, lobes spiny,
5 and subequal, or 6–10 with the secondary lobes smaller. Corolla 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-lobed. Thecae ± distinct.
Style-lobes slightly unequal. Nutlets apically rounded, hairy or
smooth. Two species in the Maritime Alps and Cyprus.
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.
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, Tourist’s Fl.: 295. 1850.
Moluccella fedtschenkoana (Kudr.) Ryding, comb. nov. ≡
Otostegia fedtschenkoana Kudr., Fragm. K Monogr. Otostegia: 28. 1939.
Acanthoprasium integrifolium (Benth.) Ryding, 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 Mast.
1874 ≡ Harmsiella Briq. in Engler & Prantl, Nat. Pflanzenfam., 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 (Prain) Hedge & Rech. 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 younger homonym
of a genus name in Tiliaceae, and proposed Harmsiella as a new
482
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. Fedtsch.) Ryding, comb. nov. ≡ Otostegia bucharica B. Fedtsch. in Izv. Imp. Bot. Sada Petra
Velikago 15: 2. 1915.
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 ≡ Harmsiella 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 (Prain)
Hedge & Rech. f. in Rechinger, Fl. Iranica 150: 345. 1982.
Moluccella sogdiana (Kudr.) Ryding, 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 Gard. Misc. 3: 880.
1833, nom illeg., non Nees 1832 ≡ Alajja Ikonn. in Novosti
Sist. Vyssh. Rast. 8: 274. 1971 ≡ Susilkumara Bennet, Indian 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, subequally 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, emarginate to almost entire, lateral lobes prominent, rounded or
emarginate. Nutlets apically truncate or subtruncate. 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 (Hedge) Ryding, comb. nov. ≡ Lamium
nepalense Hedge in Notes Roy. Bot. Gard. Edinburgh 29:
30. 1969.
Eriophyton rhomboideum (Benth.) Ryding, comb. nov. ≡ Erianthera rhomboidea Benth. in Hooker’s J. Bot. Kew Gard. Misc.
TAXON 60 (2) • April 2011: 471–484
3: 880. 1833 ≡ Lamium rhomboideum (Benth.) Benth., Labiat.
Gen. Spec.: 509. 1834 ≡ Alajja rhomboidea (Benth.) Ikonn.
in Novosti Sist. Vyssh. Rast. 8: 274. 1971 ≡ Susilkumara
rhomboidea (Benth.) Bennet, Indian Forester 107: 433. 1981.
= Erianthera anomala Juz. in Bot. Mater. Gerb. Bot. Inst. Komarova 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 species, but Hedge (1990) included it as a synonym
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 (Hedge) Ryding, comb. nov. ≡ Lamium
tuberosum Hedge in Notes Roy. Bot. Gard. Edinburgh 25:
49. 1963.
= Lamium gilongense H.W. Li, Fl. Xizangica 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.
After four of the five sections are excluded from the genus,
Budantsev’s description in Harley & al. (2004) has to be modified 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, NY, O, S,
TEX, UPS, US, and WU for permission to sample from herbarium
specimens used in this study, Richard G. Olmstead for a DNA sample
of Gomphostemma javanicum, Janet Barber for DNAs of Sideritis,
Philip D. Cantino for providing silica-dried material of Chelonopsis
moschata, and Charlotte S. Bjorå for providing silica-dried material 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 from the Research Council of Norway) that has supported
the present paper. Liv Borgen, Anne K. Brysting, Inger Nordal and
Marte Holten Jørgensen are thanked for valuable comments on the
manuscript. Finally, we are most grateful to Richard G. Olmstead,
two anonymous reviewers and the editor, Mary Endress, for positive,
useful and rapid feedback on our submitted manuscript.
Bendiksby & al. • Lamioideae─a taxonomic update
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