Molecular Phylogenetics and Evolution 109 (2017) 33–58
Contents lists available at ScienceDirect
Molecular Phylogenetics and Evolution
journal homepage: www.elsevier.com/locate/ympev
Time to split Salvia s.l. (Lamiaceae) – New insights from Old World Salvia
phylogeny
Maria Will ⇑, Regine Claßen-Bockhoff
Johannes Gutenberg-Universität, Institut für Spezielle Botanik, Anselm-Franz-von-Bentzel-Weg 2, 55099 Mainz, Germany
a r t i c l e
i n f o
Article history:
Received 25 May 2016
Revised 22 December 2016
Accepted 30 December 2016
Available online 3 January 2017
Keywords:
Salvia
Polyphyly
Classification
Phylogeny
Sections
Parallel evolution
a b s t r a c t
Aims: Salvia L. is widely known as the largest genus in the mint family. A morphological modification of
the androecium (lever-like stamens) was used to support this genus. However, molecular data revealed
that Salvia is polyphyletic. Since phylogenetic studies largely underrepresented Old World Salvia species,
we filled this gap and combined new data with existing sequences. The aim of our study was the identification of well-supported clades that provide the basis for evolutionary and taxonomic conclusions.
Methods: We included ITS data (internal transcribed spacer) from 220 Salvia species, 86 of which were
sequenced for the first time. Additionally, the highly variable plastid marker rpl32-trnL was sequenced,
providing new data for 100 Salvia species. These sequences were combined with the accessions available
from GenBank. Old World Salvia is represented herein with 57% of its species. The two datasets were analyzed separately using BI and ML approaches.
Results: Our data confirm that Salvia is polyphyletic with four distinct evolutionary lineages (Clade I-IV),
including five additional genera. The clades strongly reflect the geographical distribution, i.e., Clade IV
(East Asia), Clade III (Southwest Asia to Northern Africa), and Clade II (America). The origin of Salvia s.
s. (Clade I) is most likely Southwest Asia. A high degree of parallel character evolution was identified
in most of the Old World sections. Based on our results, we reconstructed the evolution and biogeography
of Salvia s.l. and propose to split this large group into six genera, each supported by geographical distribution, morphology, and karyology.
Conclusion: Salvia s.l. is a polyphyletic group that was originally regarded as a genus because its species
share a derived stamen structure. However, phylogenetic data clearly indicate that this floral trait and
other morphological characters evolved in parallel. Our study illustrates that the combination of different
data sets allows a comprehensive reconstruction of taxa and characteristic evolution, both of which are a
precondition for future revision.
Ó 2016 Published by Elsevier Inc.
1. Introduction
1.1. Salvia L. – a highly polyphyletic genus
Large genera, including Astragalus, Euphorbia, Minuartia, Psychotria, Ranunculus and Solanum, have repeatedly been found to be
non-monophyletic (Bruyns et al., 2006; Dillenberger and
Kadereit, 2014; Emadzade et al., 2010; Hörandl et al., 2005;
Nepokroeff et al., 1999; Osaloo et al., 2003; Rastipishe et al.,
Abbreviations: NW, New World; OW, Old World; SW, Southwest; BLB, Bering
Land Bridge; NALB, North Atlantic Land Bridge; MRCA, Most Recent Common
Ancestor.
⇑ Corresponding author.
E-mail addresses: maria.will@uni-oldenburg.de (M. Will), classenb@uni-mainz.
de (R. Claßen-Bockhoff).
http://dx.doi.org/10.1016/j.ympev.2016.12.041
1055-7903/Ó 2016 Published by Elsevier Inc.
2011; Weese and Bohs, 2007; Zimmermann et al., 2010). In contrast to paraphyly (Hörandl, 2006; Hörandl and Stuessy, 2010;
Zander, 2008), polyphyly is unacceptable to describe natural
groups and demands taxonomic consequences. Because it is rather
unpopular to split well-known genera, new concepts for classification should not be introduced lightly (e.g., Kress et al., 2005;
Kučera et al., 2013; Mansion, 2004; Whitten et al., 2007) but also
should not be delayed for practical or sentimental reasons.
Salvia is well-known for its ornamental, medicinal, hallucinogenic, or esculent plants (Clebsch, 2008; Froissart, 2008). To date,
approximately 980 species have been recognized, most of which
are restricted to the New World (NW1), the most important center
of species diversity (Appendix A, see Wester and Claßen-Bockhoff,
2011; Bedolla-García et al., 2011; Martínez-Gordillo and LozadaPérez, 2011; Turner, 2011; Véliz Pérez and Quedensley, 2011;
34
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Fernández Alonso, 2012; González-Gallegos and Castro-Castro,
2012; González-Gallegos et al., 2012a, 2012b; Iltis et al., 2012;
Sagástegui Alva and Rodríguez Rodríguez, 2012; GonzálezGallegos, 2013; González-Gallegos and Castro-Castro, 2013;
Gonzáles-Gallegos and Gama-Villanueva, 2013; González
Gallegos et al., 2013; Fragoso-Martínez and Martínez-Gordillo,
2013; Turner, 2013; Fernández-Alonso, 2014; González-Gallegos,
2014; González-Gallegos and Aguilar-Santelises, 2014; LaraCabrera et al., 2014; Fragoso-Martínez et al., 2015; GonzálezGallegos, 2015; Bedolla-García and Zamudio, 2015). Further hotspots of species richness are located in the Old World (OW2),
where approximately 350 spp. are found (Appendix B, see Thulin,
1993; Vural and Adigüzel, 1996; Van Jaarsveld, 1999; Dönmez,
2001; Haber and Semaan, 2004; Hamazaoğlu et al., 2005; Yıldırımlı
and Ertekin, 2008; Ilçim et al., 2009; Thulin, 2009; Celep and Dog
˘an, 2010; Kahraman et al., 2011b; Zhu et al., 2011; Hu et al.,
2013; Takano et al., 2014; Celep et al., 2015).
The major characteristic supporting Salvia as a genus is the
peculiar modification of its stamens. The latter have a lever-like
structure and function, a characteristic that has also been
described as a key innovation for the genus (Claßen-Bockhoff
et al., 2004b). Together with the calyx and corolla morphology,
‘stamen types’ have been consistently used to separate Salvia from
other genera (Harley et al., 2004). However, despite this morphological support, the phenotypic diversity (Plate 1A–S) in Salvia
has repeatedly caused conflicting opinions regarding classification
(Table 1).
1.2. Taxonomic history
In the early nineteenth century, various attempts were made
towards a classification of Salvia with the introduction of different
subgenera and sections (Bentham, 1832–36, 1848, 1876; Boissier,
1879; Briquet, 1897; Bunge, 1873). A split of the genus into various
genera was even proposed (Rafinesque, 1837). These early treatments were largely based on morphology and only partly on the
species distribution (e.g., Bunge, 1873).
Rafinesque (1837) accepted 28 small genera instead of one
large Salvia genus. Unfortunately, his specimens were not preserved, and little information on the characteristics supporting
and separating these genera are currently available (Merrill,
1949; Von Hagen, 1947). Nonetheless, the names have been published and must be considered for future taxonomic revisions. As
a first example, Pleudia Raf. has recently been resurrected (Will
et al., 2015). Two further names proposed by Rafinesque are under
consideration for resurrection, i.e., for the Calosphace and Audibertia clades, both of which are now a subject of taxonomic revision
(Mark Porter, personal communication).
Bentham (1832–36), in contrast, proposed 14 sections based on
morphology and distribution. Later, he arranged the species in 12
sections (Table 2; Bentham, 1848). In a third study, Bentham
(1876) included Salvia in the tribe Monardeae, together with Perovskia Karel, Dorystaechas Boiss et. Heldr., Meriandra Benth., Salviastrum Scheele, Audibertia, Rosmarinus L., Monarda L., Blephilia
Raf., and Ziziphora L. He established four subgenera, Salvia, Sclarea,
Calosphace and Leonia, to further classify the 12 sections (Table 2).
The geographical distribution and morphology of the calyx, corolla
and stamens were the main arguments for his classification.
Bentham’s 1876 classification is still used today. Six species, originally placed in a separate genus, i.e., Audibertia Benth., were later
accepted as Salvia sect. Audibertia Benth. (Epling, 1938).
Bunge (1873) basically revised the OW sections accepted by
Bentham (1848), in particular the Southwest (SW3) Asian ones.
His classification is only partially comparable to the one of
Bentham (1876) since he accepted different taxonomic groups
(Table 2).
Boissier (1879) adopted the subsectional system of Bunge with
a few changes (Table 2).
Briquet (1897) provided the most recent subgeneric classification and arranged approximately 500 Salvia species in 17 sections
and eight subgenera (Table 2). He considered Salviastrum, Polakia
Stapf and Ramona Greene (=Audibertia Benth. sensu Boissier,
1879) as genera distinct from, but closely related to, Salvia
(Table 1). Together, these genera were included in the tribe
Salvieae.
Many subsequent studies have addressed the infrageneric classification of Salvia s.l. (e.g., Dos Santos, 1991, 1995, 1996; Dos
Santos et al., 2005; El-Gazzar et al., 1968; Emboden and Lewis,
1967; Epling, 1938, 1939; Espejo-Serna and Ramamoorthy, 1993;
Fernández-Alonso, 2006; Fujita, 1970; Hedge, 1974a; Hrubý,
1962; Huang and Wu, 1975; Jenks et al., 2013; Kahraman et al.,
2010, 2011a; Lippert, 1979; Neisess, 1983; Peter, 1936; Peterson,
1978; Pobedimova, 1954; Reales et al., 2004; Reisfield, 1987;
Rosúa and Blanca, 1986, 1988; Stibal, 1934, 1935; Strachan,
1982; Torke, 2000; Walker and Elisens, 2001; Wang et al., 2013;
Whitehouse, 1949).
Hrubý (1962) suggested the elevation of some subsections to
the genus level, a taxonomic approach that was also proposed by
Rafinesque (1837) more than one century earlier.
Hedge (1974a, 1982a, 1982b) revised Old World Salvia. In his
study on African Salvia (Hedge, 1974a), he referred to Bentham’s
sections and introduced ‘species groups’. The latter were based
on morphology (e.g., floral and stamen morphology) and distribution. In his later treatments of SW Asian Salvia (Hedge, 1982a,
1982b) he focused on N African/SW Asian disjunctions and discussed their relationships (Davis and Hedge, 1971; Hedge,
1974a). While the corresponding treatments provided clear
insights into the morphological relationships of Salvia in Africa,
Turkey, and Iran (Hedge, 1974a, 1982a, 1982b), a synopsis of all
OW species has remained difficult since the ‘species groups’ in
Africa and SW Asia did not correspond to each other. Within the
Flora of Turkey, ‘species groups’ were not explicitly named but
indicated by horizontal dots (Hedge, 1982a, pp. 402–403).
Hedge’s concept of ‘species groups’ not only contributed to a
better understanding of relationships in OW Salvia, but it also provided the most up-to-date infrageneric classification for the corresponding local floras.
1.3. Molecular data: a new perspective on Salvia
The first molecular studies of Salvia rejected monophyly for the
genus in its traditional circumscription (Walker et al., 2004).
Indeed, the species were highly supported in four different clades
that were closely related to Dorystaechas, Meriandra, Perovskia, Rosmarinus, and Zhumeria Rech. f. & Wendelbo. Walker et al. (2004)
revealed three clades (I-III). Later, a slight increase in sampling
placed the genus Zhumeria (Rechinger and Wendelbo, 1967) in a
derived position within one of these clades, which was thus renamed Salvia ‘clade III’ (Walker and Sytsma, 2007). Will and
Claßen-Bockhoff (2014) recognized the latter as two independent
lineages and distinguished Clade III (SW Asian Salvia species and
Zhumeria) and Clade IV (E Asian Salvia).
The existing molecular studies are either restricted to a small
subset of species or reflect the flora of a certain region (Jenks
et al., 2011, 2013; Li et al., 2013; Sudarmono, 2007; Sudarmono
and Okada, 2008; Takano and Okada, 2011; Walker et al., 2015).
Thereby, relationships between clades remain largely unresolved.
The present study adds new sequences for OW Salvia and combines
them with the existing molecular data for NW and OW Salvia. The
aim of our study is the identification of well-supported clades providing the basis for evolutionary and taxonomic conclusions.
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
35
Plate 1. Phenotypic diversity of Salvia s.l. Distribution in brackets; NW = New World, OW = Old World; A–J Clade I (Salvia s.s.; subclades based on Will and Claßen-Bockhoff,
2014); A S. scabra, B S. namaensis, C S. thermarum (all three I-A; OW); D S. roemeriana, E S. texana (both I-B; NW); F S. judaica (Salvia verticillata-group; OW); G S. canariensis, H
S. indica, I S. broussonetii (all three I-C; OW); J S. officinalis (I-D; OW); K-S species excluded from Salvia s.s.; K S. florida Benth., L S. splendens Sellow ex Wied-Neuw., M S. patens,
N S. carduacea Benth., O S. apiana (all five Clade II; NW); P S. aegyptiaca (III-A; OW); Q S. glutinosa, R S. evansiana var. evansiana, S S. chienii (all three IV; OW); Photographs: L.
Cairampoma (K), R. Claben-Bockhoff (P), P. Wester (C-E, I, L-O, Q), M. Will (A, B, F-H, J, R-S); figures not on the same scale.
36
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Table 1
Taxonomic treatment of genera closely related to Salvia. + confirmation of previous classification.
Bentham
Briquet
Rechinger and Wendelbo
(1967)
(1832–36)
(1848)
(1876)
(1897)
Meriandrac
Perovskiaa
Dorystaechasb
+
Audibertiae
Rosmarinusg
+
+
+
+
+
Salviastrumd
+
+
+
+
+
+
Ramonaf
+
Polakiah
Zhumeriai
a
b
c
d
e
f
g
h
i
Perovskia Karel (3 spp.; W-Asia).
Dorystaechas Boiss et. Heldr. (monospecific.; SW-Asia).
Meriandra Benth. (2 spp.; Ethiopia and Himalaya).
Salviastrum Scheele (4 spp.; Texas); formerly also accepted as Salvia sect. Salviastrum (Gray, 1872; Torrey, 1859).
Audibertia Benth. (originally 6 spp., NW).
Ramona Greene (California; Greene (1892) accepted representatives of Audibertia Benth. in his new genus with Ramona polystachya (Benth.) as type species.
Rosmarinus L. (monospecific; Mediterranean Area).
Polakia Stapf (monospecific; SW-Asia), P. paradoxa Stapf is synonym to Salvia aristata Aucher ex Benth. (Behçet and Avlamaz, 2009).
Zhumeria majdae Rech. f. & Wendelbo (monospecific; S-Iran).
Table 2
Subgeneric classification of the genus Salvia. Early concepts based on a broad taxon sampling are considered here; + confirmation of previous sections, - previous sectional status
not accepted; = sphace; # = species not included; § = subsection; NW = New Word; OW = Old Word; sect. = section; subg. = subgenus.
Bentham
a
b
c
d
e
f
g
h
i
j
k
l
m
n
o
p
q
r
s
Bunge
Boissier
Briquet
Distribution
(1832–36)
(1848)
(1876)
(1873)
(1879)
(1897)
Sect.
Sect.
Subg.
Sect.
Sect.
Sect.
Subg.
OW
Eusphace
+
Salvia
Eusphace Benth. p.p.a
Eusphace Benth.
Salvia Benth.
Drymo
Hymeno
+
+
Physo Bungeb
+
Hymeno p.p.c
§ Simplicifoliae
§ Pinnatae
-j
+
Hymeno Benth.
x
x
x
x
x
x
Gymno
-e
–
–
–
Horminum
Aethiopis
+
+
Sclarea
+
Clono Bungeh
Gongro Bunge
Homalo Bunge
+
-i
+
+i
+
#
#
#
Notio (Benth.) Bungeo
Eremo Bungep
#
#
#
#
+q
Plethio
+
Echino m
Pycno n
Hetero
Notio
+
+
+
+
Hemi
+
Calo
Micro
+s
-s
Leonia
Calo
–
–
+
+
Nacto Briq.d
Schraderia (Moench) Briq.
Gymno(Benth.) Briq.f
Allagospagon Maxim.g
Allagospadonopsis Briq.
x
x
Horminum (Mönch) Benth.
Stenarrhena (Don) Briq.
§
Gongro (Boiss.) Briq. j
§ Homalo (Boiss.) Briq.k
+l
Sclarea (Mönch) Benth.
x
x
x
x
x
Leonia (Llav. et Lex.) Benth.
+
+
+
+
+
+
+
Neo Briq.r
+
#
–
#
–
+
–
Viasala Briq.
Covola (Medik.) Briq.
x
x
x
x
x
Jungia (Moench) Briq.
Only S. rosaefolia Sm.
Only S. aristata Auch.
Only SW-Asian spp.
Only African spp.
Monospecific sect. Gymnosphace Benth. (S. saxicola Benth.) included in sect. Notiosphace Benth.
Monospecific (S. saxicola Benth.; India).
Monospecific (S. piasezkii Maxim.; China).
Sect. Aethiopis Benth. p.p.: species with stamen characters of sect. Aethiopis and calyx characteristics of sect. Hymenosphace; S. compressa Vahl.
Sect. Aethiopis Benth. p.p.: S. compressa (sect. Clonosphace Bunge) included in sect. Homalosphace Bunge.
Sect. Gongrosphace and Physosphace Bunge; Boissier (1879) transferred S. aristata from Physosphace Bunge to § Gongrosphace (Boiss.) Briq.
Sect. Homalosphace and Clonosphace Bunge.
Syn.: Gallitrichum Jord. et Fourr.
Monospecific (S. carduaca Benth.), recognized as genus Audibertia by Bentham (1848).
Only two NW spp.: S. columbariae Benth. and S. leonia Benth.
Sect. Notiosphace Benth. p.p.: only E-Asian and Australian spp.
Sect. Notiosphace Benth. p.p.: only SW-Asian spp.
Notiosphace Benth. ex parte [. . .] Calyx [. . .] interdum ut in Pletiosphace dorso bisulcate (p. 592).
Only S. nilotica which was placed in Heterosphace by Bentham (1848).
Originally two NW spp.: S. occidentalis Swartz and S. misella Humb. et Kunth.; Bentham (1848) included sect. Microsphace Benth. in sect. Calosphace Benth.
NW
x
x
x
x
x
37
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
2. Materials and methods
2.1. Taxon sampling
Plant material was collected in the field or obtained from herbaria and living collections. As far as possible, specimens from
the natural distribution of the corresponding species were used.
Data for Salvia s.l. and ten additional genera are provided (Table 3).
Five of these genera represent the out-groups, while Dorystaechas,
Meriandra, Perovskia, Rosmarinus, Zhumeria, and Salvia are considered the in-group based on current molecular data (Table 4).
All major lineages encompassing Salvia species identified in the
study by Walker and Sytsma (2007) are represented, including
Clade II. Since this particular lineage was repeatedly supported
by several molecular studies (Jenks et al., 2011, 2013; Walker
et al., 2004, 2015; Walker and Sytsma, 2007; Will and ClabenBockhoff, 2014), it is only sampled herein using a small subset of
species. The number of Salvia species accepted in NW (Appendix
A) and OW Salvia (Appendix B) is based on literature research
and a reduction of synonyms for doubtful taxa (Alziar, 1988–
1993; Behçet and Avlamaz, 2009; Boissier, 1879; Clement, 1999;
Codd, 1985; Cooke, 1908; Cramer, 1981; Feinbrun-Dothan, 1978;
Table 3
Plant material included in this study. Sequences generated in this study are indicated by a DNA accession number (acc. No.); ACECR = Academic Center for Education Culture and
Research (Iran); BG HH = Botanical Garden Hamburg (Germany); cult. = cultivated; PSL METU = Plant Systematics Lab. Department of Biological Sciences, Middle East Technical
University, Ankara (Turkey); RBGE = Royal Botanical Garden Edinburgh (UK); herbarium acronyms according to Index Herbariorum; locality: given only explicitly for material
collected in the natural distribution area. Afg = Afghanistan; Azerb = Azerbaijan; Canary Isl = Canary Islands; Kurd = Kurdistan; Mad. = Madagascar; Pak = Pakistan; Taj = Tajikistan; Uzb = Uzbekistan; Yug = Yugoslawia.
Taxon
Locality
Collinsonia canadensis L.
Dorystaechas hastata Boiss. & Heldr. ex Benth.
Anatolia
Hyptis laniflora Benth.
Horminum pyrenaicum L.
Lepechinia calycina (Benth.) Epling ex Munz
Lepechinia lamiifolia (Benth.) Epling
Lepechinia mexicana (S. Schauer) Epling
Melissa axillaris (Benth.) Bakh.f.
Melissa officinalis L.
Meriandra bengalensis (Konig ex Roxb.) Benth.
Perovskia atriplicifolia Benth.
Rosmarinus officinalis L.
Salvia absconditiflora Greuter & Burdet (syn. S. cryptantha
Montbret & Aucher ex Benth.)
S. adenocaulon H.P.Davis
S. adenophylla Hedge & Hub.-Mor.
S. aegyptiaca L.
Anatolia
S. aerea Levl.
SW China
S. aethiopis L.
Armenia
Armenia
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
africana-caerulea L.
africana-lutea L.
albicaulis Benth
albimaculata Hedge & Hub.-Mor
amplexicaulis Lam.
anatolica Hamzaoğlu & Duran
aramiensis Rech.fil.
areysiana Deflers
argentea L.
ariana var. ariana Hedge
arisanensis Hayata
aristata Aucher
Anatolia
Anatolia
S Africa
S Africa
Anatolia
Yug
Anatolia
Anatolia
Yemen
Italy
Afg
Taiwan
Iran
Iran
S. atrocyanea Epl.
S. atropatana Bunge
Anatolia
Voucher
DNA
GenBank acc. No.
Collector with number (herbaria)
acc.
No.
rpl32-trnL
nrITS
JBW 958
Raiche s.n. (UCBG 1984.0696)
Albach D6-4 (University Oldenburg)
Cult. RBGE1972-0177D
Cult. RBGE1972-0177D
B. Drew 41
Isolate K36721
Cult. RBGE 1997-2109a
M. Will 63 (MJG 003069)
Trusty 28 (FTG, ex hort. Fairchild Tropical Gard.)
Drew 197
B. Drew 178
B. Drew 164
D. E. Boufford et al. 24526
M. Will 64 (MJG 003068)
B. Drew 70
JBW 2527 (cult. USA/WIS)
Lavranus & Newton 15796 (MO 2633828)
M. Will 65 (MJG 003070)
–
–
213
–
–
–
–
–
390
–
–
–
–
–
388
–
–
–
472/
374
–
389
–
92/
258
69
70
204
–
–
–
–
–
281
–
230
81
1
71
299
72
73
282
57
297
–
417
–
289
–
74
–
JQ669291
KJ747319
JQ669302
–
JQ669317
–
JQ669315
KJ747327
–
JQ669324
JQ669325
JQ669326
JQ669334
KJ747325
JQ669335
–
–
–
DQ667248
JQ669087
KJ584248
DQ667252
HQ418845
–
JF301548
DQ667257
KJ584247
AY506654
JF301344
JF301348
JF301350
JQ669114
KJ584249
JF301353
DQ667291
DQ667329
KJ584242
JQ669352
KJ747310
JQ669364
KU578211
DQ667223
KJ584197
DQ667241
KU563839
KU578149
KU578218
KJ747314
–
–
–
–
–
KU578150
–
KJ747271
KJ747273
KJ747274
KU578219
KU578151
KU578221
KU578247
KJ747315
KJ747299
KU578152
–
KJ747264
JQ669365
–
–
KU578153
KU563828
KU563789
KJ584245
DQ667285
EU169469
EU169466
EU169467
KC473229
KJ584163
DQ667272
KJ584204
KJ584205
KJ584206
KU563790
KU563829
KU563840
KU563791
–
KJ584164
KU563843
AB295100
–
DQ667280
KJ584244
DQ667270
KU563841
JBW 2524 (cult. USA/WIS)
M. Will 66 (MJG 003071)
JBW 2558 (cult. USA/WIS)
S. Bagherpour 435 (PSL METU)
F. Celep 1251 (PSL METU)
F. Celep 1500 (PSL METU)
M. Kuschewitz s.n. (cult. BG HH)
McLeish 3728 (E)
Isolate S0609
Isolate S0610
Isolate S0618
Isolate 511190202
J. Hellwig s.n. 26/6/02 (MJG 009919)
J. Hellwig s.n. 26/6/02 (MJG 009919)
P. Wester 319 (MJG 041401)
P. Wester 342 (MJG 041393)
P. Wester 340 (MJG 041403)
F. Celep 1032 (PSL METU)
D. Podlech 28360 (M 56468)
S. Bagherpour 304 (PSL METU)
F. Celep 1400 (PSL METU)
Thulin 8472 (UPS)
R. Claben-Bockhoff s.n. Mai 2002 (MJG)
D. Podlech & K. Jarmal 30029 (M 52749)
H. Okada et al. 5677
Y. Ajani 1569 (ACECR)
Wedelbo & Assadi s.n. (E)
Rechinger s.n. Iter Iranicum VIII, 1974 (M)
Isolate x140
A. Kahraman 1570 (PSL METU)
(continued on next page)
38
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Table 3 (continued)
Taxon
S. aucheri ssp. canescens (Boiss. & Heldr.) Celep,
Kahraman & Dogan
Locality
Anatolia
S. aurita L.fil.
S. austriaca Jacq.
S.
S.
S.
S.
S.
S.
axillaris Moe. et Sesse & Benth.
aytachii Vural & Adıgüzel
ballsiana (Rech.fil.) Hedge
bariensis Thulin
blepharochlaena Bedge & Hub.-Mor.
bowleyana Dunn
S.
S.
S.
S.
S.
brachyantha (Bordz.) Pobed.
brevilabra Franch.
broussonetii Benth.
bucharica M.Popov
bulleyana Diels
Austria
Mexico
Anatolia
Anatolia
Somalia
Anatolia
SW China
Anatolia
SW China
Taj
China
S. cabulica Benth.
Afg
S. cadmica Boiss.
S. caespitosa Montb. & Auch. ex Benth.
Anatolia
Anatolia
S. canariensis L.
S.
S.
S.
S.
S.
candelabrum Boiss.
candidissima ssp. occidentalis Hedge
candidissima Vahl.
cassia Rech.fil.
castanea Diels.
f. castanea Diels.
Anatolia
Anatolia
China
China
f. glabrescens Stib.
f. pubescens Stib.
S. cavaleriei Lévl.
var. simplicifolia Stib.
S. cedronella Boiss.
S. ceratophylla L.
S. chamelaeagnea Berg.
S. chienii E.Peter
S. chinensis Benth.
S. chionantha Boiss.
S.
S.
S.
S.
chloroleuca Rech.fil. & Aell.
chrysophylla Stapf
cyanescens Boiss. & Bal.
cyclostegia Stib.
SW China
Anatolia
Anatolia
rpl32-trnL
nrITS
F. Celep 1245 (PSL METU)
239
KU578248
KJ584193
Archibald 7670 (E)
P. Wester 324 (MJG 041405)
–
11/
424
–
280
–
377
79
283
80
–
–
83
–
29
270
250
–
KJ747276
DQ667286
KJ584218
–
KJ747261
JQ669366
KU578220
KU578215
KJ747316
KU578210
–
–
KU578154
–
KJ747293
KU578222
KU578203
DQ667323
–
DQ667294
–
KU563841
–
KU563793
EF373645
EU592037
KU563844
EF373636
KJ584226
KU563794
KU563780
–
–
KU578223
KU578224
KJ584189
DQ667287
KU563795
KU563796
KJ747295
–
KJ747255
KJ747300
–
KU578190
–
–
–
–
–
–
–
–
–
–
KU578146
KJ747289
KJ747322
–
–
KU578155
KJ584227
DQ667256
KJ584190
KJ584165
DQ667261
KU563845
KU563781
KC473231
EU169463
EU169464
EU169460
EU169461
EU169462
KC473232
EF373618
KU563797
–
KJ584210
KJ584250
DQ132868
EF373647
KU563846
KU578156
KU578157
KU578158
–
–
–
–
–
–
KJ747308
–
KJ747263
–
KJ747312
KU578159
KU578204
–
–
–
–
–
KJ747296
–
KU578197
KU578226
KU563847
KU563848
KU563849
EU169465
EU169475
KC473234
KU563782
DQ667332
EF373640
KJ584187
DQ667258
KJ584176
DQ132865
–
KU563830
KU563783
DQ667255
DQ132869
EF014348
EU169473
KC473235
KJ584179
DQ667290
KU563882
–
R. Claben-Bockhoff s.n. 2004 (cult. BG Mz)
R. Claben-Bockhoff s.n. 12.06.2003 (MJG)
JBW 3038 (WIS)
S. Bagherpour 412 (PSL METU)
A. Kahraman 1505 (PSL METU)
Thulin 9424 (UPS)
F. Celep 1217 (PSL METU)
L. Zhang 05008 (TRISAU, China)
A. Kahraman 1572 (PSL METU)
Y.H. Zhou 06011 (TRISAU, China) §
M. Will 33 (MJG 041537)
M.G. Pimenov, E.V. Kljuykov, I. Mukumov 113 (MW)
Sino-Amer. Bot. Exped. No 412; 24 June 1984 (HUH
144417)
Freitag 137713 (M)
Ghafoor & Goodman 5148 (E)
F. Celep 1426 (PSL METU)
F. Celep 1544 (PSL METU)
M. Will 46 (MJG 041565)
Cult. RBGE 1986–0478
M. Will 42 (MJG 041557)
F. Celep 1487 (PSL METU)
Cult. RBGE 1999-2202A
F. Celep 1411 (PSL METU)
Boufford et al. 33005 (HUH 286714)
Isolate 511190205
Isolate S0617
Isolate S0619
Isolate S0612
Isolate S0621
Isolate S0623
Isolate 511190206
Z.J. Yang 06006 (TRISAU, China) §
F. Celep 1455 (PSL METU)
A. Kahraman 1378 (PSL METU)
P. Wester 314 (MJG 041407)
M. Will 61 (MJG 003066)
AnH0305-21
Iran
Anatolia
Anatolia
H. Akhani 11027 (M)
F. Celep 1464 (PSL METU)
A. Kahraman 1593 (PSL METU)
Isolate S0620
Isolate S0611/voucher S011 (TRISAU, China)
Isolate 511190209
D.E. Boufford & B. Bartholomew 24763 (HUH 144426)
Boufford & Bartholemew 24763 (MO 4026698)
Z.J. Yang 05005 (TRISAU, China) §
M. Will 34 (MJG 04155)
Cult. RGB E 1988-2283A
M. Will 96 (MJG 003100)
XingJ0305-1
E. Gamal Eldin s.n. 3.5.1991 (GOET)
F. Celep 1330 (PSL METU)
Boufford et al. 35075 (HUH 272649)
Cult. RBG Edinbourgh 1999-2200A
YunN0309-3
China
China
SW China
S. deserta Schang
S. disermas L.
(syn. S. rugosa in GenBank)
S. disjuncta Fern.
S. divaricata Montbret & Auch. ex Benth.
GenBank acc. No.
acc.
No.
F. Celep 1464 (PSL METU)
S. daghestanica Sosn.
S. deserti Dcne.
S. dichroantha Stapf
S. digitaloides Diels
DNA
Anatolia
SW China
S. cynica Dunn
Voucher
Collector with number (herbaria)
Egypt
Anatolia
China
Guatemala
Anatolia
Isolate S0605
Isolate 511190211
P. Wester 326 (MJG 041413)
Goldblatt 7500 (E)
P. Wester 296 (MJG 041288)
A. Kahraman 1591 (PSL METU)
322
–
85
86/
256
5
–
62
201
–
165
251
–
–
–
–
–
–
–
–
88
89
52
53
–
–
90/
257
308
91
93
–
–
–
248
–
–
276
–
286
–
335
94
253
–
–
–
–
–
15
–
176
97
39
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Table 3 (continued)
Taxon
Locality
S. dolomitica Codd
Voucher
DNA
GenBank acc. No.
Collector with number (herbaria)
acc.
No.
rpl32-trnL
nrITS
KJ747290
–
–
KJ747262
KU578163
KU578167
KU578227
KJ584214
DQ667322
KJ584167
KJ584166
KU563870
KU563850
KU563819
X. Fan 04001 (TRISAU, China) §
Isolate S0606
Isolate S0622
Isolate S0607
Isolate S0616
isolate 511190212
S. Bagherpour 493 (PSL METU)
F. Celep 1082 (PSL METU)
F. Celep 1373 (PSL METU)
P. Wester 490 (MJG 041430)
Strohbach 149 (E)
Sudarmono et al. Jap03/68 (BO)
Sudarmono et al. Jap05/69 (BO)
Sudarmono et al. Jap05/70 (BO)
A. Takano 091001-1(HYO)
A. Takano 091028-1 (HYO)
A. Takano 090930-3 (HYO)
82
–
267
217
177
95
96/
405
202
–
–
415
–
–
–
–
–
–
–
–
98
260
100
393
–
–
–
–
–
–
–
KU578225
–
–
KJ747323
–
–
–
–
–
–
–
–
KJ747266
KU578168
KJ747256
KJ747320
–
–
–
–
–
–
–
KU563818
EF373621
FJ593405
KJ584251
DQ132867
EF014349
EF373624
EU169468
EU169470
EU169472
EU169474
KC473236
–
KU563851
KJ584195
KU563881
DQ667281
AB295104
AB295105
AB295106
AB541120
AB541119
AB541121
F. Celep 1196 (PSL METU)
JBW 2568 (cult. USA/WIS)
M. Kuschewitz s.n. (cult. BG Mz)
JBW 2511 (WIS)
S. Bagherpour 534 (PSL METU)
H. Okada et al. 5676
A. Kahraman 1516 (PSL METU)
F. Celep 1427 (PSL METU)
P. Wester 389 (MJG 009886)
JBW 2516
R. Claben-Bockhoff 1/05 (MJG 009888)
Boufford et al. 35205 (HUH 286716)
JBW 2577
A. Kahraman 1295 (PSL METU)
A. Kahraman 1468 (PSL METU)
Rechinger 47123 (E)
J. Hellwig s.n. 6/18/02 (MJG 009920)
Isolate 511190214
F. Celep 1061(PSL METU)
A. Kahraman 1354 (PSL METU)
Y. Ajani 1600 (ACECR)
A. Kahraman 1539 (PSL METU)
M. Will 30 (MJG 041550)
(Okada) Jap03/72 (BO)
Sudarmono et al. Jap03/34 (BO)
Sudarmono et al. Jap02/33 (BO)
Sudarmono et al. Jap03/37 (BO)
Sudarmono et al. Jap01/16 (BO)
Jap02/56 (BO)
Jap03/34 (BO)
Jap03/45 (BO)
Jap03/03 (BO)
M. Will 57 (MJG 003061)
M. Kuschewitz s.n. (MJG 009325)
Isolate 511190215
101
–
214
–
102
–
103
104
375
–
40
252
–
105
242
–
–
–
106
407
419
107
447
–
–
–
–
–
–
–
–
–
409
44
–
–
–
–
JQ669367
KU578170
–
KU578216
KU578246
KU578165
–
KJ747313
KJ747324
–
KU578228
KJ747257
–
–
–
–
KU578196
KU578171
KU578172
KJ747265
–
–
–
–
–
–
–
–
–
KU578160
KU578173
–
KJ584253
DQ667250
KU563774
DQ667215
–
AB295099
–
KU563799
KU563875
DQ667216
KJ584246
KJ584252
DQ667239
KU563800
KJ584192
DQ667288
DQ667265
KC473238
KU563876
KU563876
KU563852
KU563853
KJ584191
AB266241
AB295096
AB295093
AB295094
AB295095
AB266240
AB266237
AB266238
AB266239
KJ584241
KU563831
KC473239
O. Neustrueva-Knorring 4857 (M) [as Schraderia
korolkovii (Regl. et Schmalh.) Pobed.]
A. Takano 090704-2 (HYO)
A. Kahraman 1575 (PSL METU)
323
–
KU563801
–
108
–
KU578245
AB541114
KU563820
S. dominica L.
Cyprus
S. engelmannii A.Grey
S. eriophora Boiss. & Kotschy
S. euphratica Montb. & Aucher ex Benth.
Anatolia
Anatolia
P. Wester 321 (MJG 041411)
JBW 3200 (cult. USA/WIS)
A. Seregin, D. Sokoloff, M. Remizova A-211 (MW)
M. Kuschewitz s.n. (MJG 009323)
P. Wester 360 (MJG 009885)
A. Kahraman 1581 (PSL METU)
A. Kahraman 1585A (PSL METU)
(syn. S. cerino-pruinosa var. pilosa)
S. evansiana Hand.-Mzt.
Anatolia
SW China
A. Kahraman 1530B (PSL METU)
X. Fan 04002 (TRISAU, China) §
var. evansiana Hand.-Mzt.
S. flava Forrest ex Diels
M. Will 55 (MJG 003060)
YunN0309-4
SW China
var. flava Forrest ex Diels
var. megalantha Diels
S.
S.
S.
S.
S.
S.
freyniana Bornm.
frigida Boiss.
fruticosa Miller
funerea Jones
garipensis E.Meyer ex Benth
glabrescens Makino
Anatolia
Anatolia
Anatolia
California
Japan
Japan
Japan
var. glabrescens Makino
var. purpureomaculata (Makino) K.Inoue ex T.Shimizu
S. glutinosa L.
S.
S.
S.
S.
S.
S.
greatai Brandegee
halophila Hedge
hayatana Makino
hedgeana Dönmez
heldreichiana Boiss. ex Bentham
henryi Grey
S.
S.
S.
S.
S.
herbanica A.Santos & M.Fernández
heterochroa Fern.
hians Royle
huberi Hedge
hydrangaea Benth.
(syn. S. dracocephaloides in NCBI)
S. hylocharis Stib.
S. hypargeia Fisch. & Mey.
S.
S.
S.
S.
S.
hypoleuca Benth.
indica L.
interrupta Schousb.
isensis Nakai ex Rara
japonica Thunb.
var. japonica Thunb.
Anatolia
USA
Anatolia
Anatolia
Anatolia
Texas
USA
Canary Isl
China
Anatolia
Anatolia
Armenia
Anatolia
Anatolia
Iran
Anatolia
Japan
Japan
Japan
Japan
Japan
Japan
Japan
Japan
Japan
S. judaica Boiss.
S. jurisicii Košanin
S. kiaometiensis f. pubescens Stib.
S. korolkovii Rgl. & Schmalh.
Tian Shan
S. koyamae Makino
S. kronenburgii Rech.fil.
Anatolia
(continued on next page)
40
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Table 3 (continued)
Taxon
S. komarovii Pobed. (syn. S. trautvetteri Rgl. var.
zarawschanica Lipsky)
S.
S.
S.
S.
S.
S.
S.
S.
S.
kurdica Boiss. & Hohen ex Benth.
lanata Roxb.
lanceolata Lam.
lanigera Poir.
leriifolia Benth.
leucodermis Baker
liguliloba Sun
limbata C.A.Meyer
lutescens var. crenata (Makino) Murata
Locality
Voucher
DNA
GenBank acc. No.
Collector with number (herbaria)
acc.
No.
rpl32-trnL
nrITS
Russia
Neutrueva-Knorring & Tzetkova s.n. 1953 (M)
313
–
KU563868
Anatolia
Iraq/Kurd
NW Pak
S Africa
N Africa
Iran
Mad
Simon s.n. (M)
Rechinger 11637 (M)
Rechinger 30.587 (M)
P. Wester 1129 (NBG)
A. El-Banhawy 11 (University Ismailia, Egypt)
Rechinger 50987 (M)
Clement, Phillipson & Rafamantanantsoa 2137 (E)
Anatolia
Japan
A. Kahraman 1571 (PSL METU)
(Tsukaya) Jap04/73 (BO)
S. Fuse 4556 (HYO)
(Sudarmono et al.) Jap05/74 (BO)
Seto G. 1-X-2005 (OSA)
A. Takano 090702-1(HYO)
Cult. BG Mz 200764650
A. Kahraman 1540 (PSL METU)
Podlech & Jarmal 29.817 (M 52671)
F. Celep 1020 (PSL METU)
321
288
326
264
198
303
348
–
109
–
–
–
–
–
451
110
290
111
–
KU578212
–
KJ747277
–
KU578194
KJ747280
–
KU578174
–
–
–
–
–
KU578166
KU578229
KU578191
KU578230
KU563776
KU563821
KU563878
KJ584201
KJ584185
KU563878
KJ584220
EU592036
KU563854
AB266243
AB353206
AB266242
AB295097
AB541125
KU563873
–
–
KU563802
268
KU578201
KU563880
246
325
–
265
212
112
–
–
–
–
–
–
–
–
–
–
113
395
183
114
316
162
115
296
78
435
117
436
64
–
–
–
–
–
–
–
–
–
274
287
224
48
399
185
–
–
–
–
–
420
–
KU578231
JQ669368
KJ747297
KJ747307
KU578169
–
–
–
–
–
–
–
–
–
–
KU578175
–
KU578198
KU578195
–
KJ747283
KU578232
–
KJ747281
KJ747284
–
KJ747258
–
–
–
–
–
–
–
–
–
–
KU578205
KU578193
KU578176
–
KU578233
KU578199
–
JQ771324
JQ669369
JQ771326
–
KU578177
KU563785
KU563805
DQ667220
KJ584184
KJ584171
KU563855
DQ667264
EF373590
EF373597
EF373604
EF373606
EF373609
EF373611
EF373612
EU169480
EU169481
KU563856
KU563885
KU563884
KU563869
KU563857
KJ584208
–
KJ584200
KJ584234
KJ584217
KU563827
KJ584229
KU563777
AB295103
AB295101
AB295102
AB541117
AB541118
AB541113
AB541123
AB541122
AB541116
KU563786
KU563833
KU563832
KU563834
KU563803
KU563883
DQ667225
–
JF301355
–
KC473251
–
var. lutescens (Roidz.) Koidz.
Japan
var. stolonifera G.Nakai
S. lyrata L.
S. macrochlamys Boiss. & Kotschy
S. macrosiphon Boiss.
_
S. marashica Ilçim,
Celep & Doğan
Anatolia
Afg
Anatolia
S. margaritae Botsch.
S.
S.
S.
S.
S.
maximowicziana Hemsl.
maymanica Hedge
mellifera Greene
merjamie Forsk.
microstegia Boiss. & Bal.
(S. verbascifolia in GenBank)
S. milthiorrhiza Bunge
f. alba C.Y.Wu & H.W.Li
var. miltiorrhiza Bunge
S. modesta Boiss.
S. mohavensis Greene
S. moniliformis Fern.
S. montbretii Benth.
S. moorcroftiana Wall. ex Benth.
S. muirii L.Bolus
S. multicaulis Vahl.
S. namaensis Schinz
S. napifolia Jacq.
S. nilotica (Juss. ex) Jacq.
Tajuk SSR,
Turkestan
China
Afg
USA
Armenia
Anatolia
Armenia
E China
N China
NE China
SW China
N China
NE China
NE China
Anatolia
California
Mexico
Anatolia
Afg
Anatolia
SW Africa
Anatolia
S. nipponica Miq.
Japan
var. nipponica Miq.
as var. kisoensis
var. trisecta (Matsum.) Honda
S. nubicola Wall. ex Sweet
S. nutans L.
C Nepal
C Russia
S. nydeggeri Hub.-Mor.
S. oaxacana Fern.
S. officinalis L.
Anatolia
S. oligophylla Auch. ex Benth.
Iran
M.G. Pimenov, E.V. Kljuykov, M.G. Vasilyeva, L.P.
Tomkovich, T.V. Lavrova 127-1 (MW)
Boufford et al. 35285 (HUH 226267)
Moh. Amin 154 (M 52655)
JBW 2550 (WIS)
M. Will 83 (MJG 003113)
J. Hellwig s.n. (MJG 009884)
F. Celep 1539 (PSL METU)
J. Hellwig s.n. (MJG 009884)
L. Zhang 05001 (TRISAU, China)
L. Zhang 05002 (TRISAU, China)
L. Zhang 05005 (TRISAU, China)
L. Zhang 05006 (TRISAU, China)
L. Zhang 05007 (TRISAU, China)
H.Q. Yu 05001 (TRISAU, China)
H.Q. Yu 05001 (TRISAU, China)
Isolate S0627
Isolate S0625
F. Celep 1543 (PSL METU)
P. Wester 517 (MJG 041380)
A. Espejo & M. Crone 21 (MJG 040167)
A. Kahraman 1381 (PSL METU)
Anders 3627 (M 52651)
P. Wester 328 (MJG 041409)
S. Bagherpour 282 (PSL METU)
W. Giess & M. Müller 14319 (M)
P. Wester 330 (MJG 041415)
M. Will 28 (MJG 041552)
F. Celep 1109 (PSL METU)
M. Will 49 (MJG 041538)
U. Hecker g3186 (MJG 003079)
H. Okada et al. 5665
Sudarmono et al. Jap03/66 (BO)
H. Okada et al. 5667
A. Takano 090701-2 (HYO)
Y. Ibaragi s. n. (HYO)
N. Fujii s. n. (HYO)
A. Takano 090617-1 (HYO)
A. Takano 090617-8 (HYO)
M. Ogawa 13452 (HYO)
A. Suchorukow s.n. IX. 2009 (MW)
A. Suchorukow s.n. VII. 2001 (MW)
M. Will s.n. (MJG 041554)
M. Will 40 (MJG 041553)
F. Celep 1491 (PSL METU)
P. Wester 259 (MJG 040630)
JBW 2580 (cult. USA/WIS)
Voucher 2160
M. Palma s.n. UCBG 7.0083
Voucher 2153 HFFBU
Isolate 511190230
Y. Ajani 1569 (ACECR)
41
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Table 3 (continued)
Taxon
S. omeiana Stib.
S. omerocalyx Hayata
var. prostrata Satake
S. pachystachys Trautv.
S. palaestina Benth.
S. paohsingensis C.Y.Wu
S. patens Cav.
S. pauciflora Kunth
Locality
SE China
Anatolia
Anatolia
SW China
S. penstemonoides Kunth & Bouché
S. persepolitana Boiss.
S.
S.
S.
S.
S.
phlomoides ssp. phlomoides Asso
pilifera Benth.
pinnata L.
pisidica Benth.
plebeia R.Br.
S. plectranthoides Griff.
S.
S.
S.
S.
poculata Náb.
polystachya Cav.
potentillifolia Boiss. & Heldr. ex Benth.
pratensis L.
S. pratii Hemsl.
S. przewalskii Maxim.
Texas
Iran
Morocco
Anatolia
Anatolia
Anatolia
Afg
Japan
SW China
China
Anatolia
Anatolia
C Russia
China
SW China
S. pterocalyx Hedge
S. pygmaea Matsum.
var. simplicior Hatus. ex T.Yamaz.
S. quezelii Hedge & Afzal-Rafii
S. radula Benth.
S. ranzaniana Makino
S. recognita Fisch. & Meyer
S. repens Burch. ex Benth.
S. cf. repens Burch. ex Benth.
S. reuterana Boiss.
S. rhytidea Benth.
S. ringens Sm.
S. roborowskii Max.
Afg
S. roemeriana Scheele
USA
Texas
Anatolia
Anatolia
E Azerb
Iran
S. rosifolia Sm.
S. russellii Benth.
S. sahendica Boiss. & Buhse
S. scabiosifolia Lam.
S. scabra L.
S. schimperi Benth.
S. schizochila Stib.
S. schlechteri Briq.
S. sclarea L.
S. sclareoides Brot.
S. serico-tomentosa Rech.fil.
S. sessilifolia Baker
Anatolia
S Africa
Anatolia
Iran
NE Afg
SW China
Yemen
Anatolia
Armenia
Anatolia
Mad
Voucher
DNA
GenBank acc. No.
Collector with number (herbaria)
acc.
No.
rpl32-trnL
nrITS
Z.J. Yang 05001 (TRISAU, China) §
A. Takano 070523–1 (HYO)
A. Takahashi 4596 (HYO)
A. Takahashi 4601 (HYO)
A. Takano 091001–3 (HYO)
A. Kahraman 1443 (PSL METU)
F. Celep 1083 (PSL METU)
Isolate 511190231
Cult RBGE 1973–9197
Isolate S0615/voucher S015 (TRISAU, China)
Isolate 511190233
Isolate 511190232
JBW 2578 (cult. USA/WIS)
P. Wester 386 (MJG 041327)
Sh. Zarre, S. Mashayekhi, F. Taeb, A .Pirani & H. Moazeni
35213 (MSB 116594)
R. Vogt 10336 & Ch. Oberprieler 4784 (B 100145114)
A. Kahraman 1506 (PSL METU)
F. Celep 1416 (PSL METU)
F. Celep 1457 (PSL METU)
Podlech 30610 (M 52986)
Sudarmono et al. Jap04/75 (BO)
L. Zhang 05010 (TRISAU, China)
Isolate 511190233
Boufford et al. 37470 (HUH 272906)
Isolate S0624
A. Kahraman 1560 (PSL METU)
Breedlove & Mahoney 72286 (UC)
F. Celep 1457 (PSL METU)
A. Suchorukow s.n. VII 2003 (MW)
Isolate S0628
Ho et al. 2084 (HUH 144453)
Cult. RBGE 1993-2067A
YunN0309-1
H.F. Guo 2017272 (PE)
–
–
–
–
–
120
400
–
–
–
–
–
–
376
324
–
–
–
–
–
–
KJ747304
–
JQ669370
–
–
–
–
KU578162
KU578178
EF373642
AB353203
AB353204
AB353205
AB541124
KU563804
KJ584175
KC473252
DQ667253
EU169476
KC473254
KC473253
DQ667221
KU563871
KU563858
337
121
122
123
312
–
–
–
247
–
124
–
126
275
–
249
–
–
–
–
–
–
349
–
–
128
328
–
153
61
437
295
294
209
–
–
–
–
465
154
155
271
421
416
55
310
466
–
31
244
278
–
–
208
156
332
KJ747309
KU578208
KU578217
KU578234
–
–
–
–
KU578207
–
KU578179
JQ669371
KU578235
KU578180
–
KU578206
JQ669372
–
–
–
–
–
KU578200
–
–
KU578249
–
–
KU578236
KJ747282
–
KU578181
KU578182
KU578213
–
–
–
–
–
KU578209
KU578148
KU578183
KU578184
KU578237
KJ747285
–
–
–
KJ747286
KJ747305
–
JQ669373
–
–
KU578238
–
KJ584186
–
KU563798
KU563806
KU563788
AB295107
EF373648
KC473255
KU563787
EU169479
KU563859
JF301356
KU563807
KU563835
EU169486
KU563784
DQ667254
DQ132862
EF053400
EF014346
EF373627
EU169471
–
AB295098
AB541126
KU563808
KJ584180
AB287375
KU563808
KJ584232
KJ584231
KU563860
KU563861
KU563810
EF373630
EU169477
DQ667289
DQ667211
KU563872
–
KU563824
KU563778
KU563862
KU563811
KJ584233
KJ584174
KJ584168
KC473273
KJ584235
KJ584162
KU563775
DQ667222
KC473274
KU563836
KU563822
KJ584224
Z.J. Yang 06005 (TRISAU, China) §
Isolate S0613
P. Wendelbo, I. Hedge & L. Ekberg W8550 (E 00253001)
H. Okada et al. 5671
A. Takano 100111-1 (HYO)
F. Celep 1626 (PSL METU)
Germishuizen 3950 (MO)
Okada 5698
S. Bagherpour 380 (PSL METU)
M. Will 50 (MJG 041931)
P. Wester 325 (MJG 041412)
D. Podlech & Sh. Zarre 55240 (MSB 89758)
Podlech 12466 (M)
M. Kuschewitz s.n. May 2004 (MJG 009332)
Z.J. Yang 06008 (TRISAU, China) §
SBQ 852 (E)
JBW 2515 (WIS)
P. Wester 350 (MJG 041332)
A. Kahraman 1470 (PSL METU)
A. Kahraman 1542 (PSL METU)
Ilkka Kukkonen 7951 (MW)
Y. Ajani 1576 (ACECR)
M. Will 67 (MJG 003072)
M. Will 37 (MJG 041549)
Podlech 36057 (M 55003)
M. Will 72 (MJG 003099)
511190253
P. Wester 323a (MJG 041416)
F. Celep 1492 (PSL METU)
J. Hellwig s.n. 23.06.2002 (MJG 010799)
JBW 2527 (cult. USA/WIS)
Isolate 511190254
M. Kuschewitz s.n. June 2004 (MJG 009334)
F. Celep 1403 (PSL METU)
Jongkind & Rapanarivo 929 (MO 4870099)
(continued on next page)
42
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Table 3 (continued)
Taxon
S.
S.
S.
S.
S.
S.
S.
S.
S.
Locality
smyrnaea Boiss.
somalensis Vatke
spinosa L.
staminea Benth.
stenophylla Burch. ex Benth.
substolonifera Stibal
suffruticosa Benth.
suffruticosa x bracteata Banks & Sol.
summa A.Nelson
Voucher
DNA
GenBank acc. No.
Collector with number (herbaria)
acc.
No.
rpl32-trnL
nrITS
Egypt
Anatolia
S Africa
F. Celep 1053 (PSL METU)
M. Will 77 (MJG 003119)
A. El-Banhawy 14 (University Ismailia, Egypt)
Max Nydegger 43701 (M 106730)
Burgoyne & Snow 4805 (MO 5649981)
Anatolia
Anatolia
Texas
USA
Anatolia
A. Kahraman 1527 (PSL METU)
A. Kahraman 1414 (PSL METU)
JBW 1972 USA (WIS)
P. Wester 373 (MJG 041338)
A. Kahraman 1568 (PSL METU)
C Russia
Anatolia
Morocco
Anatolia
Texas
Texas
A. Suchorukow s.n. VIII 1994 (MW)
S. Bagherpour 440 (PSL METU)
W. Lippert 25355 (M)
F. Celep 1425 (PSL METU)
P. Wester 362 (MJG 041477)
P. Wester 362 (MJG 041477)
P. Wester 336 (MJG 041398)
Podlech 43384 (M 54979)
F. Celep 1759 (PSL METU)
S. Bagherpour 502 (PSL METU)
Cult. MJG 200764580
Breckle 4963 (E)
A. Kahraman 1532
Z.J. Yang 06008 (TRISAU, China) §
Dickoré 14538 (MSB 144138)
YunN0309-5
133
340
199
307
330
–
402
157
–
190
118
–
273
136
304
158
191
–
23
314
138
139
336
–
166
–
291
–
–
–
–
413
67
141
150
51
167
211
160
77
231
–
161
147
–
KU578239
KJ747311
KJ747303
–
KJ747260
–
KU578240
KU578241
–
KU578164
KJ747292
–
–
KU578147
KJ747270
KU578242
KJ747267
–
KJ747288
–
KU578188
–
KU578214
–
KU578243
–
–
–
–
–
KJ747306
–
KJ747298
KU578192
–
KU578161
KU578185
KU578186
KU578202
KJ747268
–
KU578244
KU578187
–
KU563812
KJ584240
KJ584173
KU563863
KJ584237
EF373646
KU563813
–
DQ667217
KU563874
KJ584181
EU169485
KJ584177
KU563864
KJ584228
KU563814
KJ584199
DQ667321
KJ584239
KJ584169
KU563865
KU563815
KU563816
DQ667283
–
EF373633
KU563779
DQ132870
EF014347
EF373614
EU169478
KJ584170
KJ584182
KJ584183
KU563866
KU563826
KU563825
KU563837
KU563838
KU563879
KJ584198
DQ667320
KU563817
KU563842
AB541115
–
148
–
–
–
–
422
–
–
–
KU578189
–
–
–
–
KJ747317
JQ669381
–
EU169485
KU563867
EF373615
EF014344
DQ132866
EU169482
KJ584243
DQ667336
DQ667335
Anatolia
S. sylvestris L.
(syn. S. tesquicola Kiok. & Pobed.)
S. syriaca L.
S. taraxacifolia Hook.fil.
S. tchihatcheffii (Fisch. & Hey.) Boiss.
S. texana (Scheele) Torr.
S.
S.
S.
S.
thermarum Van Jaarsv.
tingitana Etl.
tobeyi Hedge
tomentosa Miller
Morocco
Anatolia
Anatolia
S.
S.
S.
S.
trichocalycina Benth.
trichoclada Benth.
tricuspis Franch.
trijuga Diels
Anatolia
SE China
China
S. veneris Hedge
S. verbenaca L.
Cyprus
Syria
Anatolia
Anatolia
S. vermifolia Bedge & Huber-Morath
S. verticillata
ssp. amasiaca (Freyn & Bornm.) Bornm.
S. virgata Jacq.
S. viscosa Jacq.
S. vvendenskii E.V.Nikitina
S. whitehouseii Alziar
Anatolia
Anatolia
Anatolia
Kirgisiya
Texas
Texas
Anatolia
Anatolia
S. wiedemannii Boiss.
S. xanthocheila Boiss. ex Benth.
S.
S.
S.
S.
x sakuensis Naruh. & Hihara
x sylvestris
yosgadensis Freyn et Bornm.
yunnanensis Wright
Zhumeria majdae Rech.fil. & Wendelbo
Isolate S0608
Foley, M.J.Y. 1701 (E)
W. Licht SYR 307 (MJG 003082)
F. Celep 1408 (PSL METU)
S. Bagherpour 521 (PSL METU)
M. Will 32 (MJG 041555)
F. Celep 1540 (PSL METU)
F. Celep 1513 (PSL METU)
F. Celep 1647 (PSL METU)
Lažkov, G.A. s.n. 2006-06-09 (W 2007-14397)
P. Wester 352 (MJG 041389)
P. Wester 352 (MJG 041389)
F. Celep 1361 (PSL METU)
A. Kahraman 1573 (PSL METU)
A. Takano 090704-3 (HYO)
Anatolia
SW China
S. Bagherpour 441 (PSL METU)
X. Fan 04003 (TRISAU, China) §
Iran
YunN0309-2
Isolate S0604
F. Sharififar 1651 (ACECR)
Wendelbo 15793 (V 21730)
Ghazi s.n.(V 01176)
Table 4
Number of species and accessions per marker. With respect to the recent molecular findings the ‘in-group’ includes Salvia s.l. and the five non-Salvia genera Dorystaechas,
Meriandra, Perovskia, Rosmarinus, and Zhumeria; NW = New World; OW = Old World; number of Salvia species sequenced for the first time in brackets.
nrITS
rpl32-trnL
Genera
Species
Accs.
Genera
Species [new]
Accs.
Outgroups
Ingroup
Non-Salvia
Former Salvia
NW
OW
5
6
5
1
–
–
8
222
5
217
19
198
13
343
11
332
25
307
5
5
4
1
–
–
7
165
4
161
15
146
10
176
7
169
15
154
Total
11
230
356
10
172
[86]
[4]
[82]
[100]
[5]
[95]
186
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Greuter et al., 1986; Harvey et al., 1912; Hedge, 1957, 1959, 1960,
1961, 1964, 1966, 1972a, 1972b, 1974a, 1980, 1982a, 1982b,
1982c, 1985, 1988, 1998, 2001; Hedge and Lamond, 1968; Huang
and Wu, 1975, 1978; Li and Hedge, 1994; Migahid, 1978;
Mouterde, 1983; Nikitina, 1962; Ohwi, 1984; Peter, 1936;
Pobedimova, 1954; Post, 1933; Rechinger fil, 1943; Santos and
Fernandez, 1986; Stewart, 1972; Stibal, 1934, 1935; Sun, 1977;
Thiébaut, 1953).
2.2. DNA extraction, amplification, and sequencing
Total genomic DNA was obtained from silica dried or herbarium
leaf material. DNA was extracted according to the manufacturer’s
protocol for the NucleoSpinÒ plant DNA extraction kit
(Macherey-Nagel, Düren, Germany). The standard 25-lL PCR reaction mix consisted of 2 mM MgCl2, 200 lM dNTPs, 1 pM primer,
0.025 U/lL Taq polymerase, and 0.5–1.0 lL of DNA extract in the
reaction buffer provided by the polymerase manufacturer. The
PCR reactions were carried out in Biometra T3 and PTC 100 MJ
Research thermocyclers using the following program: 60 s at
94 °C (pre-treatment), 35 cycles of 20 s at 94 °C, 30 s at 55 °C,
60 s at 72 °C, and a post-treatment (80 s at 55 °C and 8 min at
72 °C). The whole internal transcribed spacer region was
sequenced as a single piece using ITS-A and ITS-4 primers (Noyes
and Rieseberg, 1999; White et al., 1990). For chloroplast sequences,
we used rpl32 and trnLUGA primers (Shaw et al., 2007). All PCR
products were purified according to the manufacturer’s protocol
using either ExoSAP-IT PCR Product Clean-up (Affymetrix UK
Ktd., Wooburn Green, UK) or the NucleoSpinÒ Extract II kit
(Macherey-Nagel, Düren, Germany). Cycle sequencing was performed using ABI Prism BigDye Ready Reaction Mix (Applied
Biosystems, Foster City, California, USA) with the same primers
used for the PCR amplifications. Products were purified with
SephadexTM G50 (VWR International GmbH, Darmstadt, Germany)
and sequenced on a 16-capillary ABI 3130xl automated sequencer
(Life Technologies GmbH, Darmstadt, Germany) at Johannes
Gutenberg-University Mainz (Germany).
2.3. Sequence alignment and phylogenetic analyses
Sequencing was conducted in two directions. Forward and
reverse sequences were edited manually, merged into consensus
sequences using SequencerTM 4.1.2. (GeneCodeCorp., Ann Arbor,
Michigan, USA) and aligned manually in McClade4.1 (Maddison
and Maddison, 2000). Ambiguously aligned regions were identified
manually and excluded from the analyses. Partitions were defined
for the ITS dataset before the best-fit models of nucleotide substitution were selected with jModeltest 2.1.1 (Darriba et al., 2012).
The maximum likelihood (ML) search, bootstrapping (BS; RAxMLHPC BlackBox v.7.4.4; Stamatakis, 2006; Stamatakis et al., 2008)
and Bayesian inference (BI; MrBayes v.3.1.2 on XSEDE; Ronquist
and Huelsenbeck, 2003) were performed using the CIPRES Science
Gateway v.3.3 server (Miller et al., 2011). For BI, we ran four Markov chains simultaneously for 40 million generations to analyze
the datasets. Two independent runs were performed with sampling every thousandth generation. The burn-in (10%; 4.000) was
determined with Tracer v.1.5 implemented in BEAST (Drummond
and Rambaut, 2007) to generate a 50% majority rule consensus
trees with posterior probabilities (PP) using MrBayes v.3.1.2.
Absent partitions were coded as missing data (‘?’). Nuclear (ITS)
and plastid (rpl32-trnLUGA) data were analyzed separately to identify incongruences. For the calculation, accessions with a 100%
identical sequence were reduced to one haplotype. This is indicated in the text and illustrations by a slash separating the accession numbers.
43
3. Results
3.1. Phylogenetic reconstructions (Fig. 1)
The two simplified topologies for Salvia s.l. (Fig. 1) illustrate the
major clades identified based on nuclear and plastid data. Four
highly supported clades, including Salvia species and additional
genera (Clade I–IV), were identified in the ITS dataset (Fig. 2):
(1) Clade I (Salvia s.s.), (2) Clade II (most NW Salvia + Dorystaechas + Meriandra), (3) Clade III (SW Asian Salvia with Zhumeria)
and IV (E Asian Salvia) (Fig. 1). Within Clade I (Figs. 1 and 3), four
major lineages were identified: (1) subclade I-B, (2) subclade I-A,
(3) S. taraxacifolia, the S. verticillata group, subclade I-C, and
S. leriifolia as one weakly supported clade (PP = 0.95), and (4)
subclade I-D.
Phylogenetic reconstructions based on the plastid data support
the same major lineages but are better resolved (Figs. 1 and 4).
Clades II, III, and IV form one clade (PP = 1.00/99% BS). A sister relationship of Clade II and IV is only found in the ML analysis (84% BS).
Clade I is found in trichotomy with Rosmarinus and Perovskia.
Together, these three branches are highly supported as one clade
(PP = 1.00/98% BS).
The plastid marker suggests a sister relationship of subclade I-C
and S. leriifolia, which was not found in the ITS dataset. Together,
the two are sisters to subclade I-D, but this relationship is not supported by the Bayesian analysis (90% BS) (Fig. 1). Both, ML and BI
make up subclade I-B, which is sister to a clade formed by S.
taraxacifolia, the S. verticillata group, and subclade I-A. In contrast
to the ITS tree, subclade I-B is only weakly supported in the ML
analysis of the cp dataset (76% BS).
3.1.1. nrITS dataset (Figs. 2 and 3)
Clade IV (Fig. 2B; PP = 1.00/100% BS) includes all E Asian species
that fall into three distinct subclades, i.e., (1) IV-A (30 spp./85
accs.), (2) IV-B (16 spp./47 accs.), and (3) IV-C (S. plebeia; 4 accs.).
Within subclades IV-A and B, some terminal groups are wellsupported, but the relationships among them are unresolved.
A similar pattern is observed for Clade III (Fig. 2A; PP = 1.00/99%
BS), which contains two major lineages: (1) Zhumeria, which is sister to S. margaritae (78% BS), and (2) a branch (PP = 1.00/98% BS)
that splits in three species-poor subclades (III-A, B, and C).
Clade II (Fig. 2A; PP = 1.00/100% BS) includes Dorystaechas and
Meriandra in a polytomy with an American clade of Salvia species,
comprising all members of the sects. Calosphace Benth. (subclade
II-A) and Audibertia (Benth.) Epling (subclades II-B and II-C).
Clade I (Fig. 3; PP = 1.00/80% BS) represents Salvia s.s. It contains all members of the Salvia sect. Aethiopis Benth. (I-C and S. leriifolia), Hemisphace Benth. (S. verticillata-group), Heterosphace
Benth. (I-A, I-B), Hymenosphace Benth. (I-A, I-C, I-D), Pletiosphace
Benth. (I-C), and all species recognized in the genus Salviastrum
Scheele (I-B). The ITS data highly support 137 spp./177 accs. nested
in Clade I (Fig. 3) with three highly supported subclades, i.e., (1) ID, (2) I-B, and (3) I-A, which are sister to an unresolved and weakly
supported clade with containing S. taraxacifolia, I-C, S. leriifolia, and
the S. verticillata group.
Subclade I-A contains two species from E Africa (S. nilotica and
S. somalensis) and all Madagascan and South African species, except
one accession of S. garipensis derived from GenBank. The clade is
poorly resolved with only a few small terminal clades supported,
of which one comprises the Madagascan endemic S. sessilifolia
and S. leucodermis.
Subclade I-B is composed of NW Salvia species with Salvia lyrata as sister to a clade with two well-supported subclades (Fig. 3).
Another highly supported subclade, the Salvia verticillatagroup (Europe, SW Asia), is found in a polytomy with S. taraxacifo-
44
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Fig. 1. Overview of the phylogenetic trees based on nuclear (nrITS) and chloroplast (rpl32-trnL) data. Clades containing Salvia species were reduced to black triangles and
highlighted by grey boxes; light grey = Salvia s.s.; dark grey = Clades II, III, and IV; non-Salvia genera highlighted in bold; only support values P75% (BS) and P0.95 (PP) are
illustrated; sequences derived from GenBank (NCBI) are indicated by accession numbers.
lia (Northern Africa, Maroco), S. leriifolia (Madagascar) and subclade I-C (Fig. 3).
Subclade I-C (Fig. 3) represents the Salvia sects. Aethiopis Benth.
and Pletiosphace Benth., with one representative of sect. Hymenosphace Benth. (S. canariensis). The relationships remain largely
unresolved except for seven subclades with taxa from Central
and SW Asia, the Canary Islands, S Africa, and the Circum Mediterranean Area.
Subclade I-D (Fig. 3) is highly supported and contains 39 spp.
(49 accs.) from S Europe, N Africa, and SW and Central Asia.
3.1.2. rpl32-trnL-dataset (Fig. 4)
As in the nuclear dataset, Clade IV (all E Asian samples), Clade
III (SW Asian Salvia and Zhumeria), and Clade II (NW Salvia and
Dorystaechas) are highly supported. Together, these three clades
form a monophylum with Clade III as sister to the remainder.
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
45
Fig. 2. Phylogenetic tree of Salvia s.l. based on ITS data. A Clade I (Salvia s.s.) and Clade IV were reduced to black triangles; B resolved topology for Clade IV; only support
values P70% (BS) and P0.95 (PP) are illustrated; two species (S. chienii DQ132868 and S. evansiana FJ593405) most likely misplaced in the tree are indicated by #; large
bar = taxa listed by Bentham (1848), medium-sized bar = sectional placement according to more recent treatments of the corresponding taxa, e.g., for E Asian (Stibal, 1934–
35; Sun, 1977) and SW Asian species (Bunge, 1873), small bar = classification assumed in this study.
46
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Fig. 3. Phylogenetic tree of Salvia s.s. (Clade I) based on ITS data. Only support values P70% (BS) and P0.95 (PP) are illustrated; four species (S. disermas DQ667290, S.
garipensis DQ667281, S. anatolica 72, and S. absconditiflora 258) that are likely misplaced in the tree are indicated by #.
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
47
Fig. 4. Phylogenetic tree of Salvia s.l. based on rpl32-trnL data. Non-Salvia genera are highlighted (bold); only support values P70% (BS) and P0.95 (PP) are illustrated.
48
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Within Clade III, two subclades with Salvia species (III-A, III-B)
are found in a trichotomy with Zhumeria. Subclade III-A represents
Salvia sect. Eremosphace Bunge distributed from the Canary Islands
throughout N Africa to the Arabian Peninsula and SW Asia. Within
this clade, S. deserti is highly supported as sister to the remainder
(Fig. 4). The four species nested in subclade III-B are restricted to
SW and Central Asia. The placement of S. margaritae in one clade
with S. vvedenskii, S. pterocalyx, and S. aristata (Fig. 4) slightly differs from the one suggested by nuclear data. Here, S. margaritae
is sister to Zhumeria instead of being grouped with the corresponding Salvia species (78% BS; Fig. 2A).
American Salvia species representing sects. Calosphace and
Audibertia are highly supported in Clade II, where they are found
in a trichotomy with the OW genus Dorystaechas. In contrast to
the ITS data, S. greatai, S. funerea (both II-B), and S. mellifera (II-C)
form one clade representing Salvia sect. Audibertia (PP = 0.95/82%
BS), which is sister to Clade II-A (Calosphace; PP = 1.00/84% BS).
Clade I (Salvia s.s.) is found in a trichotomy with Perovskia and
Rosmarinus. The topology of Clade I slightly differs from the one
suggested by nuclear data. The sister relationship of subclades IC (including S. leriifolia) and I-D proposed by the ML analysis, for
example, is not supported by the ITS data (Fig. 1). Furthermore,
the plastid data propose that subclades I-B and I-A (including the
S. verticillata group and S. taraxacifolia) are one clade. Within Clade
I, all subclades except I-B are highly supported.
In contrast to the topology based on the ITS data, subclade I-A
is closely related to S. taraxacifolia and the S. verticillata group.
Together with S. nilotica, and S. somalensis, these three lineages
form one large unresolved clade. Within the S African and Madagascan branch, two clades are identified (Fig. 4).
Subclade I-B corresponds to the one suggested by the ITS data
but has lower statistical support.
Subclade I-C contains 59 taxa (61 accs.) from SW and Central
Asia, Europe, the Canary Islands, and S Europe. They fall into three
major lineages: (1) S. leriifolia, (2) a polytomy of S. phlomoides ssp.
phlomoides, S. hypargeia, S. montbretii, and S. daghestanica, and (3) a
large unresolved clade containing 54 taxa in four subclades.
The plastid data do not confirm the monophyly of S. microstegia
and S. sclarea, which is contradicts the ITS data for S. sclarea. Further incongruences concern single species nested in subclade I-C,
i.e., S. jurisicii is sister to S. nutans based on the ITS data (Fig. 3)
but sister to S. virgata based on the cp data (Fig. 4). In contrast,
the nuclear data support S. virgata and S. viscosa as one clade.
Subclade I-D contains 47 taxa (50 accs.), and although resolution is low, four clades can be identified within the polytomy: (1)
S. maymanica and S. aytachii, (2) S. multicaulis and S. marashica,
(3) S. interrupta and S. candelabrum, and (4) one highly supported
clade encompassing eight SW Asian taxa. For the following species,
the sequences were treated as one haplotype: (1) S. anatolica, S. blepharochleana, S. absconditiflora, and S. fruticosa, (2) S. caespitosa, S.
kurdica, S. ringens, and S. tomentosa, (3) S. aramiensisa and S. pilifera,
and (4) S. ballsiana and S. rosifolia.
4. Discussion
Our data support the polyphyly of Salvia s.l. suggested by previous studies (Walker et al., 2004; Walker and Sytsma, 2007; Moon
et al., 2010; Drew and Sytsma, 2012; Will and Claben-Bockhoff,
2014) using a much broader sampling, especially for the OW taxa.
We confirm that Salvia species fall in four clades (Clade I-IV). Old
World species are nested in three distinct clades (Clade I, III, and
IV), and NW Salvia are placed in two independent evolutionary lineages, i.e., Clade II and subclade I-B. Although the relationships are
not resolved at the species level, we are able to distinguish well-
defined clades, thus providing a molecular background for future
revisions (see Will et al., 2015).
4.1. Taxonomic conclusions
Based on current knowledge, we propose to split the former
genus Salvia into six genera (Fig. 5). It is not the intention of the
present paper to provide a taxonomic revision and key. Instead,
we identify clades and name them based on previously published
generic names to indicate that they could be elevated to generic
rank after revision. This process is helpful even now, since the
use of existing clade names (I, II, III, ‘III’, and IV), as well as the
name Salvia itself, are confusing. Since the type species of the
genus, S. officinalis (Jarvis, 2007), is nested within Clade I, this clade
represents Salvia s.s.
4.1.1. Salvia s.s. (Clade I)
Salvia s.s. is split into several well-supported subclades with
morphologically heterogeneous species (Plate IA-J). Subclade I-B
contains only NW species (Plate ID-E), while all other subclades
include exclusively OW species.
4.1.1.1. Salvia verticillata group. This subclade represents the Salvia
sect. Hemisphace Benth. Within Clade I, this is the only section
sensu Bentham (1832–36) and subsequent taxonomic treatments
confirmed to be monophyletic. The species can be recognized by
verticillasters with many (up to 40) small flowers (Plate 1F). The
latter have blue corollas with falcate upper lips and almost completely reduced lower lever arms lacking thecae. These stamens
can no longer act as staminal levers (Hildebrand, 1865; ClabenBockhoff et al., 2004a).
4.1.1.2. Subclade I-A. Chloroplast data suggest a close relationship
of the Salvia verticillata group and subclade I-A. Regarding phenotypic diversity, the latter is by far the most heterogeneous
within Salvia s.s. It is characterized by a broad range of stamen
modifications, ranging from levers with fertile lower thecae to
completely reduced ones (Will and Claßen-Bockhoff, 2014). Species are restricted to the African continent and Madagascar. Floral
characters such as corolla size, shape, and color are extraordinarily
diverse among species (Plate IA-C), most likely reflecting adaptation to the pollinator diversity in Southern Africa (Will and
Claßen-Bockhoff, 2014).
4.1.1.3. Subclade I-B. The NW species nested in subclade I-B represent two different taxonomic groups. Salvia species representing
Salviastrum Scheele are supported as monophyletic, while representatives of Salvia sect. Heterosphace Benth. (I-B) are paraphyletic with respect to Salviastrum (Figs. 3 and 4).
Based on their restricted distribution in the southern states of N
America (Fig. 6B), chromosome numbers (2n = 28; Walker and
Elisens, 2001; Ward, 1984), and floral morphology (i.e., calyx, corolla, stamen characters), subclade I-B should be newly described
on a subgeneric rank of Salvia s.s. The idea to combine Salviastrum
and the NW representatives of Salvia sects. Heterosphace has be
previously proposed by Torrey (1859), Walker et al. (2004), and
Whitehouse (1949), although there are marked differences in the
flowers (Plate 1D and E).
4.1.1.4. Subclade I-C. All species that are nested in this subclade
represent Salvia subgen. Sclarea Benth. (Salvia sect. Aethiopis
Benth. and sect. Plethiosphace Benth.) excluding S. canariensis
(Salvia sect. Hymenosphace Benth.). All sect. Aethiopis is within subclade I-C except for S. leriifolia, which is found in a polytomy with
subclade I-C (Fig. 3).
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
49
Fig. 5. Phylogenetic tree for Salvia s.l. illustrating well-supported clades identified in both datasets. Support values for ITS above and for rpl32-trnL below the branches;
+ = maximal support (PP = 1.00/100% BS); dotted lines = nodes that are only supported by plastid data; number of taxa represented in the corresponding clade and total
number of species assumed in this group (Appendix C) indicated in brackets; light grey bars = OW species; dark grey bars = NW species.
The monophyly of this subclade has been previously suggested
by different molecular markers and smaller sample sets (Walker
et al., 2004; Walker and Sytsma, 2007; Will and Claben-Bockhoff,
2014). However, the relationships within subclade I-C remain
unresolved, and further studies are needed to address sectional
delimitations. Species of subclade I-C are characterized by reduced
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M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Fig. 6. Distribution of Salvia s.l. and related genera. A: Note the disjunct distribution of S. glutinosa (IV-A) and the remainder of subclade IV-A and IV-B; B: major subclade of
Salvia s.s.; subclade I-B slightly overlapping with Clade II-A; C: distribution of S. plebeia (IV-C); distribution of subclade III-B likely extending further into C Asia; D: non-Salvia
genera closely related to Salvia s.s.: Perovskia atriplicifolia and Rosmarinus officinalis; Clade II: Dorystaechas hastata and Meriandra bengalensis; Clade III: Zhumeria majdae.
Distribution based on Behçet and Avlamaz (2009), Bokhari and Hedge (1976), Hedge (1960, 1986), Hedge and Lamond (1968), Hedge and Wendelbo (1978), Jenks et al.
(2013), Nikitina (1962), Mabberley (2008), Meusel et al. (1978), Sales et al. (2010), local floras (see material and methods) and IPNI, http://.plants.usda.gov/core/profile?
symbol=SARO3 (accessed 03.07.2014); template of the map provided by the German earth science portal (www.mygeo.info).
lower lever arms lacking fertile thecae and falcate corollas (Plate 1G-I). They have a disjunct distribution with few species
restricted to S Africa and the majority restricted to Europe and
SW and Central Asia (Fig. 6B).
According to Bentham (1832–36), three sections were included
in Salvia subgen. Sclarea: sect. Aethiopis Benth, sect. Horminum
Benth., and sect. Plethiosphace Benth. However, the placement of
S. canariensis (Plate 1G) in subclade I-C is in clear conflict with
the current classification. The species that was originally grouped
in Salvia subgen. Salvia Benth. sect. Hymenosphace Benth. is indeed
sister to S. broussonetii (Plate 1I) from Salvia subgen. Sclarea Benth.
sect. Aethiopis Benth. (Fig. 3). This unexpected relationship, which
has been previously discussed in greater detail by Will and
Claßen-Bockhoff (2014), reflects the parallel characteristic evolution in S. canariensis and some S African and SW Asian members
of Salvia sect. Hymenosphace (Fig. 3; I-A and I-D).
All members of Salvia sect. Plethiosphace Benth. investigated
herein are placed in subclade I-C, but the relationships between
the species remain unresolved. Salvia viridis (monotypic Salvia sect.
Horminum Benth.) is not included in the present study, but a previous molecular study (Walker et al., 2004) highly support its position in this subclade.
4.1.1.5. Subclade I-D. The resolution is low within this highly supported lineage. The two sections placed within the clade, i.e., Salvia
sect. Aethiopis Benth. and sect. Hymenosphace Benth., are nonmonophyletic (Fig. 3). Representatives of subclade I-D have fertile,
at least subfertile, thecae on the lower lever arms of their stamens.
Compared with subclade I-C, the corolla of Salvia species nested in
subclade I-D is comparatively large, and the upper lip is rather
straight (Plate 1J). Furthermore, there seems to be a tendency
towards the expression of lobed or even compound leaves within
both sections.
Current data support a taxonomic concept of Salvia s.s. that is
consistent with the species distribution, as previously suggested
by Bunge (1873) and Briquet (1897).
4.1.2. Clade II
According to the cp data, the NW Clade II is weakly supported
and sister to OW Clade IV. Based on current data, we propose to
split Clade II (Fig. 5) into four different genera, i.e., Dorystaechas,
Meriandra (both OW), Lasemia Raf. (II-A; NW), and Ramona Greene
(II-B and C; both NW) (Fig. 5). Lasemia and Ramona are largely congruent with Salvia subgen. Calosphace (Epling, 1939) and Salvia
sect. Audibertia (Neisess, 1983), which was recently proposed as
Salvia subgen. Audibertia (Walker et al., 2015).
With respect to their morphology, distribution, and molecular
data (Fig. 2), it is most parsimonious to regard Dorystaechas and
Meriandra as relicts (Bokhari and Hedge, 1971; Hedge, 1986,
1992; Henderson et al., 1968; Will et al., 2015).
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
4.1.2.1. Lasemia Raf. (subclade II-A). Subclade II-A represents all
NW species formerly placed in Salvia sect. Calosphace (Dos
Santos et al., 2005; Drew and Sytsma, 2012; Jenks et al., 2013;
Walker et al., 2004, 2015; Walker and Sytsma, 2007). It is phenotypically diverse (Plate 1K-M) and extraordinarily rich in species.
Nevertheless, the following characteristics support this subclade
and its elevation to the generic rank of Lasemia Raf.: (1) species distribution ranges from the southern US to S and Central America
(Fig. 6B), (2) straight lower lever arms that lack a fertile theca,
and (3) a basic chromosome number of 2n = 22, with many polyploid species (e.g., Alberto et al., 2003; Harley and Heywood,
1992; Mercado et al., 1989; Palomino et al., 1986).
4.1.2.2. Ramona Greene (subclades II B and C). Subclades II B and C
correspond to Salvia sect. Audibertia (Benth.) Epling (see also
Walker et al., 2015). Taxa are restricted to California and Baja California (Fig. 6B) and placed in two distinct lineages: (1) Salvia sect.
Echinosphace Benth. (II-B) and (2) Salvia sect. Audibertia (Benth.)
Epling (II-C). The former is characterized by the occurrence of
toothed or even spiny leaves, many flowers arranged in compact
verticillasters, and fertile thecae on the lower lever arms (Plate 1N). The basic chromosome number in this clade is 2n = (30)
32 and/or 64 (Epling et al., 1962; Neisess, 1983).
The plastid data suggest that subclades II-B and II-C are sister to
each other (Fig. 4), which is in accordance with the classification
concept proposed by Neisess (1983).
4.1.3. Clade III
This clade is split into three subclades with Salvia species (III-A
to C), which can be distinguished based on the ITS data (Fig. 5). We
propose to recognize two distinct genera, i.e., Pleudia Raf. (subclades III-A and C) and Polakia Stapf (subclade III-B) (Will et al.,
2015).
4.1.3.1. Pleudia Raf. (subclades III-A and C). Subclades III-A and C
include species that are morphologically and ecologically closely
related and are clearly distinct from the remainder of Clade III.
Will et al. (2015) recently re-established the genus Pleudia Raf.,
which can be recognized by the combination of the following characteristics: (1) low growing, greatly branched shrubs or suffruticose herbs, often appearing as dwarf shrubs, usually <40 cm; (2)
small leaves, usually with revolute margins; (3) small flowers, usually less than 10 mm; (4) few-flowered verticillasters with shortlived flowers (Plate 1P); (5) upper lip of the corolla ± straight; (6)
stamens at least partially exposed, very short connections, lower
thecae fertile or sometimes reduced (very small or even sterile);
and (7) small nutlets.
4.1.3.2. Polakia Stapf (subclade III B). Species nested in subclade III-B
occur in dry habitats similar to the ones described for Pleudia.
However, they have been traditionally separated from Pleudia
based on their morphology and distribution (Bunge, 1873;
Briquet, 1897; Pobedimova, 1954; Will et al., 2015). To date, 16
species from Central and SW Asia belong to this group. The latter
seem to correspond to Salvia sect. Physosphace Bunge and Salvia
subgen. Macrosphace Pobed. sensu Pobedimova (1954). We sampled one of the five species from subgen. Macrosphace (S. margaritae Botsch,) and two representatives from Salvia sect. Physosphace
(S. aristata and S. vvedenskii), all of which were placed in subclade
III-B (Fig. 4). The position of S. aristata, formerly placed in Salvia
sect. Eusphace sensu Bentham, again illustrates the parallel characteristic evolution in a non-monophyletic section (Fig. 4). Molecular
data appear to support the classification introduced by
Pobedimova (1954), who underscored some morphological similarities between Salvia subgen. Macrosphace and Salvia sect. Physosphace Bunge. However, the existing delimitation of the
51
corresponding subgenus and section is not very clear and must
be refined. The following attributes are characteristic of Polakia:
(1) comparatively large corollas (P25 mm) and calyces (generally
>15 mm); (2) long pedicels (P5 mm up to 20 mm); (3) large, occasionally lobed or even compound leaves; and (4) large seeds
(Behçet and Avlamaz, 2009; Hedge, 1960, 1974b, 1982b; Nikitina,
1962; Pobedimova, 1954).
4.1.4. Glutinaria Raf. (Clade IV)
Based on morphological and molecular data, 97 species are
expected to nest in subclades IV-A and IV-B (Appendix C), with S.
plebeia being the single species representing subclade IV-C. All species of Clade IV are restricted to E Asia with only few exceptions,
e.g., S. glutinosa (Eurasia) and S. plebeia (Fig. 6C).
Clade IV is extraordinarily homogenous with respect to its basic
chromosome number of x = 8 (Afzal-Rafii, 1980; Ayyangar and
Vembu, 1984; Bir and Saggoo, 1981; Bir and Sidhu, 1980; Bir
et al., 1978; Hihara et al., 2001; Jee et al., 1989; Markova and
Ivanova, 1982; Saggoo and Bir, 1986; Sales et al., 2010; Shiuchi
and Kanemoto, 2001; Song et al., 2010; Strid and Franzen, 1983;
Sudarmono and Okada, 2008; Vir Jee and Kachroo, 1985; Vij and
Kashyap, 1975, 1976; Wang et al., 2009; Wu and Huang, 1975;
Yang et al., 2004, 2009; Zhao et al., 2006). This characteristic
strongly supports the monophyly of Clade IV.
Although it is possible to accept three distinct subclades and to
split Clade IV into three distinct genera, we propose only one
validly published name for the clade (Fig. 5) since it is not yet possible to provide a good set of characteristics (synapomorphy) for
each subclade. Regarding Clades IV-A, B, and C, the following
names merit consideration for future revision, either in the sectional or generic rank: (1) Glutinaria Raf. (subclade IV-A) with S.
glutinosa as the type species, (2) Sobiso Raf. (subclade IV-B) with
S. japonica as the type species, and (3) Notiosphace (Benth.) Bunge
corresponding to subclade IV-C.
4.1.4.1. Subclades IV-A and IV-B. Molecular data largely support the
classification sensu Stibal (1934, 1935) (Fig. 2A), with all representatives of Salvia subgen. Eusalvia Stib. sect. Eurysphace Stib.
nested in subclade IV-A. However, it remains uncertain whether
the S. substolonifera group (S. substolonifera and S. trijuga; Fig. 2B)
is closely related to the remainder of the clade. The former classification and morphology of the two species link it rather with the
species nested in subclade IV-B (Fig. 2B).
Molecular data suggest that Salvia subgen. Sclarea (Moench)
Benth. sect. Drymosphace Benth. is paraphyletic with respect to
Salvia subgen. Gymnosphace (Benth.) Stib. We recognize subclades
IV-A and IV-B and highlight the need for further molecular studies.
More parsimony-informative characteristics and a higher resolution are needed to revise Clade IV and to support it with morphological characteristics.
Based on current knowledge and the unresolved backbone of
Clade IV, we do not yet provide a morphological set of characteristics to distinguish subclades IV-A and IV-B. As in other lineages
with Salvia species, the distribution and karyology appear to be
suitable characteristics supporting the monophyly.
4.1.4.2. Subclade IV-C. Our results support previous molecular studies (Sudarmono and Okada, 2008; Takano and Okada, 2011) indicating that S. plebeia represents the only species in Salvia sect.
Notiosphace Benth. (Fig. 2B). Sales et al. (2010) provided detailed
information regarding the isolated position and taxonomic history
of S. plebeia, which appears suitable to elevate S. plebeia to generic
rank.
The relationship of S. plebeia to some other small-flowered Salvia species from E Asia originally also placed it in the section Nothiophace sensu Bentham (Bentham, 1832–36, 1848), which must be
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M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
rejected. Today, it is clear that the section sensu Bentham is polyphyletic. We strongly support the dissolution of Salvia sect. Notiosphace Benth. based on the phylogeny and species distribution, as
previously proposed by Bunge (1873). In this case, the clade should
be recognized as the genus Notiosphace (Benth.) Bunge.
4.2. Salvia in space and time – distribution and dispersal
The current topology largely reflects the species distribution. It
suggests that America was colonized twice, most likely by species
distributed in SW Asia. Walker and Sytsma (2006) suggested that
the closest relatives of the former Calosphace and Audibertia members occur in Asia. This assertion was also supported by Drew and
Sytsma (2012). However, the distribution patterns, biogeography,
and putative migration routes of species placed in Salvia s.l. raise
many questions. A precondition to answer these questions is the
calibration of a broadly sampled phylogenetic dataset.
4.2.1. Divergence time estimations
Drew and Sytsma (2012) provided an initial approach to elucidate not only the distribution of ancestral lineages but also to
determine the divergence times (Fig. 7). The authors performed
a molecular study of Mentheae and represented Salvia s.l. with five
non-Salvia genera and nine Salvia species. Although the sampling
for Salvia s.l. was restricted, some approximations concerning its
age were suggested. Drew and Sytsma (2012) conclude that all
subtribes of the Nepetoideae arose 34 million years ago (Ma).
According to the divergence interval, the most recent common
ancestor (MRCA) of Salvia s.l. existed in the late Eocene (34 Ma)
to the middle Oligocene (26 Ma). The node supporting Clades II,
III, IV, and related genera as one clade was found to have originated
approximately at the Oligocene-Miocene border (Drew and
Sytsma, 2012) (Fig. 7). This lineage is thus older than the MRCA
of Salvia s.s. (Clade I), which diversified between the middle-tolate Miocene (15–6 Ma). The MRCA of Rosmarinus and Perovskia,
which are sister to Clade I, was found to diverge most likely during
the early to middle Miocene. This age might indicate the relict status of the two genera (Will et al., 2015). The comparatively early
existence of the MRCA of Rosmarinus and Perovskia conflicts with
the age estimate proposed by Peñuelas et al. (2001). The authors
suggested that Rosmarinus evolved under Mediterranean climate
conditions, which were assumed to occur in Europe since approximately 3.2 Ma. Suc (1984) discussed an additional, more recent
‘xeric phase’ (2.3 Ma) that also caused climatic and vegetation
changes in Europe. Current data suggest that Rosmarinus either
evolved during earlier periods of aridification in its contemporary
distribution range or likely originated elsewhere before it was dispersed to the Mediterranean.
4.2.2. Fossil sites and fossil records
Age estimates are largely congruent with known fossil records
for Salvia s.l. (Table 5). However, some of them remain doubtful,
and in particular those fossils assigned to NW representatives of
Clade II are quite young (Table 5). Within the largely unresolved
subclades II-B and C (Taylor and Ayers, 2006; Walker and
Sytsma, 2006), it is quite complicated to allocate them to a certain
node. For species of subclade II-C, numerous fossil packrat middens
were recorded with age estimates spanning from the Holocene to
the late Pleistocene (Anderson and Van Devender, 1991;
Betancourt et al., 1986; Cole, 1986, 1990; King and Van
Devender, 1977; Nowak et al., 1994; Spaulding, 1983, 1990; Van
Devender, 1987; Wells, 1976). This time frame corresponds to
the postglacial vegetation change from Juniperus-dominated woodlands to desert scrubs, e.g., in the Mohave region (Wells, 1976). The
corresponding fossils (Table 5; Fig. 7) might reflect an adaptation
to increasing aridification in this region and probably supply
insights into recent ecological adaptations. However, the comparatively recent records especially are not suitable for a more detailed
fossil-based calibration of Salvia s.l. Only the oldest fossil record
assigned to NW Salvia sect. Audibertia (Table 5) allocated to the
upper Miocene of Alaska (Fig. 8A, black asterisk) (Emboden,
1964; Müller, 1981) seems to be useful for this purpose. The age
of this fossil is in accordance with the age estimate for the MRCA
of S. greatai and S. mellifera (Fig. 8) in Drew and Sytsma (2012).
Several fossil reports cited in the literature cannot be confirmed
herein, including Claben-Bockhoff et al. (2004b), Kaya and Kutluk
Fig. 7. Most recent common ancestors (MRCA) of the Mentheae subtribe. Phylogenetic tree and slightly modified dating after Drew and Sytsma (2012); grey bars = 95%
confidence intervals for estimated mean dates; numbers on branches indicate references for fossil records according to Table 5; dotted lines mark the border between
geochronological units; Ma = million years ago; Plio. = Pliocene, Quat. = Quaternary.
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
53
Table 5
Fossil records for Salvia s.l. Geochronological units are taken from literature; references for fossils are given as in italics in Fig. 7; for clade names (I–IV) and the corresponding
subclades (A–D) see Fig. 8B; abbreviations for fossilized structures (fossils): c = calyx; l = leaf; m = macrofossil; n = nutlet; p = pollen;? = data not available or not clearly indicated;
y B.P. = years before present; localityies: Am = America, W = West.
a
b
c
Clade
Taxon
Fossil
Locality
Age [y B.P.]
Reference
I
I-B
I-B ?
I-D
verticillata
lyrata
Salvia sp.
cf. officinalis
n
m
c
n
Thuringia (Germany)
Nebraska (US)
Texas (US)
Thuringia (Germany)
Plio-/Pleistocene 1.8–1.7 106
Holocene 2.000 ( 9.000)
?
Pliocene
1
2
3
4
Mai et al. (1963)a
Baker (2000)
Wells (1976)
Mai and Walter (1988)
II
II ?
II-A
II-A
II-A
II-B
II-C
II-C
II-C
II-C
II-C
II-C
II-C
II-C
II-C
Salvia sp.
Salvia sp.
cf. Salvia
pinguifolia b
pinguifolia b
Audibertia-type
cf. funerea
dorrii
dorrii
dorrii
mohavensis
mohavensis
mohavensis
mohavensis
mohavensis
m
c
p
m
m
p
m
m
m
m
p
m
m
m
l
W-USA
Texas (US)
Ecuador (S-Am)
Arizona (US)
Arizona (US)
Alaska
California (US)
California (US)
Great Basin (US)
Nevada (US)
Sonora (US)
California (US)
Colorado River (US)
California (US)
Arizona (US)
Late Holocene 670 ± 40–1.450 ± 160
?
Pleisto/Holocene 13.070 ± 270
Early Holocene 7.970
Wisconsin 12.700
Upper Miocene
Late Wisconsin 10.460
Late Wisconsin 10.260–10.210
>13.000
Mid-to-Late-Holocene 30.000
Pleisto/Holocene
Wisconsin 12.390 ± 340
>10.000
Late Wisconsin 10.460–10.210
Early Holocene 14.120–10.540
5
3
6
7
8
9
10
10
11
12
13
14
15
10
7
Betancourt et al. (1986)
Wells (1976)
Colinvaux et al. (1997)
Van Devender (1987)
Scott Anderson and Van Devender (1991)
Emboden (1964)
Spaulding (1983)
Spaulding (1983)
Spaulding (1990)
Nowak et al. (1994)
King and Van Devender (1977)
Cole (1986)
Cole (1990)
Spaulding (1983)
Van Devender (1987)
IV-A
IV-A
cf. glutinosa
cf. glutinosa
n
n
?
Alsace (France)
?
Pliocene
16
17
Geissert et al. (1990)
Teodoridis et al. (2009)
?
?
Salvia sp.
Salvia sp.
?
p
Europe
Crimea
Plio-/Pleistocene
Holocene
18
19
Mai (1995)
Cordova and Lehman (2005)
c
According to Mai and Walter (1988) the nutlet illustrated in Mai et al. (1963) is more likely Origanum vulgare L. foss.
Syn. S. ballotiflora Benth.
Pollen similar to the extant species: S. funerea, S. californica, and S. greatae.
Fig. 8. Salvia s.l. in time and space. A: Distribution of Salvia s.l., putative migration routes and fossil sites; BLB = Bering Land Bridge; D = Dorystaechas; M = Meriandra;
NALB = North Atlantic Land Bridge; P = Perovskia; R = Rosmarinus; Z = Zhumeria; white arrows indicate repeated colonization of S Africa and dispersal from the Eastern Cape to
Madagascar; hatched arrows (dark grey) indicate the repeated colonization of the Canary Islands from two different mainland sources; red arrow illustrate the dispersal from
E Asia to Eurasia reflected by S. glutinosa; black arrows correspond to dispersal events from the OW to America reflected by two distinct lineages; ? = route uncertain;
template of the map provided by the German earth science portal (www.mygeo.info). B: Simplified phylogenetic tree; nodes discussed in the text are indicated by capital
letters; colors reflect distribution areas. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
54
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
(2007), and Valiente-Banuet et al. (2006). The latter suggested a
Quaternary origin for Salvia sect. Calosphace Benth. (II-A) based
on the fruit morphology and refer to ‘a fossil-calibrated phylogeny
of Salvia’ provided by Walker et al. (2004), which is actually not
provided by the corresponding reference.
Regarding members of the Calosphace (Fig. 7: S. axillaris and relatives), it is more likely that their diversification and radiation are
correlated to the recent uplift of the Andes. In contrast to this comparatively recent putative origin, Reisfield (1987) argued that Calosphace might be derived from an OW ancestor reaching Mexico in
the Neogene. Data provided by Drew and Sytsma (2012) suggest a
comparatively old age for the MRCA of Calosphace, which is in
accordance with the hypothesis of Reisfield (1987). In contrast, a
recent diversification might be assumed for the derived lineages
within Calosphace.
4.2.3. Biogeography and dispersal
Regarding the origin of Salvia s.l., Claßen-Bockhoff et al.
(2004b) hypothesized that the group probably originated in the
OW, i.e., in the Mediterranean area. Current data support this
hypothesis for Clades I, II, and III. The authors suggest that the high
species diversity in the NW Salvia sect. Calosphace should be interpreted as a recent diversification. For Africa and America, they
hypothesized a southwards-directed migration via tropical mountain routes during the Miocene and Pliocene.
Regarding the dispersal into the New World, it remains uncertain whether species used the Bering Land Bridge (BLB4)
(Claßen-Bockhoff et al., 2004b) or the North Atlantic Land Bridge
(NALB5). Drew and Sytsma (2012) provided age estimates for the
Most Recent Common Ancestor (MRCA6) of NW Salvia nested in
Clade II and a Dorystaechas/Meriandra clade. This age estimate falls
in a time frame when both the BLB and the NALB still provided
suitable biotic connections between the OW and NW (e.g., Briggs,
1987; Gladenkov et al., 2002; Milne, 2006; Wen, 1999; Xiang
et al., 2000) (Fig. 7). Thus, it is not possible to determine the migration route that accounts for the dispersal of Clade II into the NW.
However, the BLB seems to be more likely with respect to the
Audibertia pollen fossil from Alaska, which was assigned to the
Upper Miocene (Emboden, 1964) (Fig. 8A).
Regarding the dispersal of subclade I-B progenitors into the NW,
both routes are possible. However, based on the current distribution of Clade I (Fig. 8A), one might argue that the NALB is more
likely than the BLB (compare Kadereit and Baldwin, 2012). In summary, it is likely that two colonizations of America occurred at different times and via different routes.
S Africa and the Canary Islands were also repeatedly colonized
(Will and Claßen-Bockhoff, 2014). There were two independent
dispersal events to the latter from different mainland sources,
i.e., from Clades I (Salvia s.s.) and III (Salvia s.l.). The nonmonophyly of the Canary Island species is reflected by their morphological divergence, which allows one to easily distinguish the
two lineages and recognize them as two distinct genera (Will
et al., 2015).
5. Conclusions
The present molecular and morphological data allow the reconstruction of the evolution of Salvia species, to date providing the
broadest sampling of OW Salvia. It is evident that Salvia s.l. is
highly polyphyletic, thus demanding revision. Parallelisms such
as an expanding calyx, flower shape, and even stamen construction, which were largely used as supporting characteristics for
the genus sensu lato and for sections are clearly not a reliable basis
for taxonomy and revisions. In light of the available molecular
data, we encourage a process to revise Salvia s.l. on a clade-byclade basis.
The present data provide a strong background for understanding evolutionary tendencies in the former genus Salvia. It is possible to briefly characterize the identified clades and to suggest
validly published names regarding the generic rank for each of
them. The proposed new genera largely reflect the geographic distribution, indicating that dispersal events likely triggered
speciation.
Acknowledgments
For helpful comments and discussion, we thank B. Gehrke, M.
Pirie, M.S. Dillenberger, and J.W. Kadereit (all Mainz, Germany).
We gratefully acknowledge F. Celep (Ankara, Turkey) for providing
us with species material from Turkey. Additional material was provided by D. Albach (Oldenburg, Germany), Y. Ajani (Mainz, Germany), S. Bagherpour (Ankara, Turkey), A. El-Banhawy (Reading,
UK), A. Kahraman (Ankara, Turkey), M. Kuschewitz (Mainz, Germany), A.P. Sukhorukov (Moscow, Russia), M. Thulin (Uppsala,
Sweden), and P. Wester (Düsseldorf, Germany). We thank all curators and colleagues making herbarium material available at ACECR
(Iran), B, E, EA, GOET, HUH, M, MJG, MO, MPU, MW, and PSL METU
(Ankara). Furthermore, we thank E. Martin (Konya, Turkey) for
sharing preliminary data from chromosome counts in Salvia, the
staff members of the Botanical Garden at Mainz for cultivating
plant material and N. Schmalz (Mainz, Germany) for proofreading
and helpful comments. Financial support was provided by the Faculty of Biology, Office of Gender Affairs and Equal Opportunity, the
Erasmus TM Mobility Program (all Johannes Gutenberg-University
Mainz, Germany) and the DFG Cl81/10-1. We thank the two anonymous reviewers for their constructive criticism.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.ympev.2016.12.
041.
References
Afzal-Rafii, Z., 1980. Lamiaceae. In: Löve, A. (Ed.), Chromosome Number Reports
LXVII. Taxon, vol. 29, pp. 365–366.
Alberto, C.M., Sanso, A.M., Xifreda, C.C., 2003. Chromosomal studies in species of
Salvia (Lamiaceae) from Argentina. J. Linn. Soc. (Bot.) 141, 483–490. http://dx.
doi.org/10.1046/j.1095-8339.2003.t01-1-00178.x.
Alziar, G., 1988-1993. Catalogue synonymique des Salvia L. du monde (Lamiaceae). I
à VI. Biocosme Mésogéen. Nice 5, 87–136. 6, 79–115; 6, 163–204; 7, 59–109; 9,
413–497; 10, 33–117.
Anderson, R.S., Van Devender, T.R., 1991. Comparison of pollen and macrofossils in
packrat (Neotama) middens: a chronological sequence from the Waterman
mountains of southern Arizona, U.S.A. Rev. Palaeobot. Palynol. 68, 1–28.
Ayyangar, K.R., Vembu, B., 1984. On the karyomorphological nuances between two
species of Salvia Linn. Proc. Indian Sci. Congr. Assoc., vol. 71.
Baker, R.G., 2000. Holocene environments reconstructed from plant macrofossils in
stream deposits from southeastern Nebraska, USA. Holocene 10, 357–365.
http://dx.doi.org/10.1191/095968300676039397.
Bedolla-García, B.Y., Lara-Cabrera, S.I., Zamudio, S., 2011. Two new species of Salvia
(Lamiaceae) from west central Mexico. Acta Bot. Mex., 51–63
Bedolla-García, B.Y., Zamudio, S., 2015. Four new species of Salvia (Lamiaceae) from
http://dx.doi.org/
central
Mexico.
Phytotaxa
217,
035–052.
10.11646/phytotaxa.217.1.3.
Behçet, L., Avlamaz, D., 2009. A new record for Turkey: Salvia aristata Aucher ex
Benth. (Lamiaceae). Turk. J. Bot. 33, 61–63. http://dx.doi.org/10.3906/bot-080814.
Bentham, G., 1832-1836. Salvia. In: Bentham, G. (Ed.), Labiat. Gen. J. Ridgway & Sons
Picadilli, London, pp. 190–312.
Bentham, G., 1848. Labiatae. In: De Candolle, A.P. (Ed.), Prodromus, vol. 12. Treuttel
& Würtz, Paris, pp. 262–358.
Bentham, G., 1876. Labiatae. In: Bentham, G., Hooker, J.D. (Eds.), Gen. Pl. 2. Reeve &
Co., London, pp. 1160–1196.
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Betancourt, J.L., Van Devender, T.R., Rose, M., 1986. Comparison of plant
macrofossils in woodrat (Neotoma sp.) and porcupine (Erethizon dorsatum)
middens from the Western United States. J. Mammal. 67, 266–273.
Bir, S.S., Kumari, S., Shoree, S.P., Sagoo, M.S., 1978. Cytological studies in certain
Bicarpellatae from north and central India. J. Cytol. Genet. 13, 99–106.
Bir, S.S., Saggoo, M.I.S., 1981. Cytopalynology of certain Acanthaceae and Labiatae. J.
Palynol. 17, 93–102.
Bir, S.S., Sidhu, M., 1980. Cyto-palynological studies on weed flora of cultivable
lands of Patiala district (Punjab). J. Palynol. 16, 85–105.
Boissier, E., 1879. Salvia. In: Boissier, E. (Ed.), Fl. Orient. Georg, H., Genevae et
Basileae, pp. 590–636.
Bokhari, M.H., Hedge, I.C., 1971. Observations on the tribe Meriandreae of the
Labiatae. Notes Roy. Bot. Gard. Edinb. 31, 53–67.
Bokhari, M.H., Hedge, I.C., 1976. Zhumeria (Labiatae): anatomy, taxonomy and
affinities. Iran. J. Bot. 1, 1–10.
Briggs, J.C., 1987. Developments in Palaeontology and Stratigraphy. Elsevier,
Amsterdam.
Briquet, J., 1897. Labiatae. In: Engler, H.G.A., Prantl, K.A.E. (Eds.), Nat. Pflanzenfam..
Engelmann, Leipzig, pp. 182–286.
Bruyns, P.V., Mapaya, R.J., Hedderson, T.J., 2006. A new subgeneric classification for
Euphorbia (Euphorbiaceae) in southern Africa based on ITS and psbA-trnH
sequence data. Taxon 55, 397–420. http://dx.doi.org/10.2307/25065587.
Bunge, A., 1873. Labiatae Persicae. Mem. Acad. Sci. Petersb. Ser. 7 (21), 40–53.
Celep, F., Doğan, M., 2010. Salvia ekimiana (Lamiaceae), a new species from Turkey.
Ann. Bota. Fenn. 47, 63–66. http://dx.doi.org/10.5735/085.047.0108.
Celep, F., Dirmenci, T., Güner, O., 2015. Salvia hasankeyfense (Lamiaceae), a new
species from Hasankeyf (Batman, South-eastern Turkey). Phytotaxa 227, 289–
294. http://dx.doi.org/10.11646/phytotaxa.227.3.9.
Claßen-Bockhoff, R., Crone, M., Baikova, E., 2004a. Stamen development in Salvia L.:
homology reinvestigated. Int. J. Plant Sci. 165, 475–498.
Claßen-Bockhoff, R., Speck, T., Tweraser, E., Wester, P., Thimm, S., Reith, M., 2004b.
The staminal lever mechanism in Salvia L. (Lamiaceae): a key innovation for
adaptive radiation? Org. Divers. Evol. 4, 189–205. http://dx.doi.org/10.1016/j.
ode.2004.01.004.
Clebsch, B., 2008. The New Book of Salvias: Sages for Every Garden. Timber Press,
Cambridge, UK.
Clement, R.A., 1999. Labiatae. In: Grierson, A.J.C., Long, D.G. (Eds.), Fl. Bhutan, vol. 2
(2). Royal Botanic Gardens Edinb. and the Royal Government of Bhutan, Edinb,
pp. 970–975.
Codd, L.E., 1985. Salvia. In: Leistner, O.A., (Ed.), Fl. South. Afr. 28(4) Lamiaceae.
Pretoria, Botanical Research Institute, Department of Agriculture and Water
Supply, Pretoria, pp. 79–101.
Cole, K.L., 1986. The lower Colorado River Valley: a Pleistocene desert. Quatern. Res.
25, 392–400. http://dx.doi.org/10.1016/0033-5894(86)90010-4.
Cole, K.L., 1990. Reconstruction of past desert vegetation along the Colorado River
using packrat middens. Palaeogeogr. Paleoclimatol. Palaeoecol. 76, 349–366.
http://dx.doi.org/10.1016/0031-0182(90)90120-V.
Colinvaux, P.A., Bush, M.B., Steinitz-Kannan, M., Miller, M.C., 1997. Glacial and
postglacial pollen records from the Ecuadorian Andes and Amazon. Quatern.
Res. 48, 69–78. http://dx.doi.org/10.1006/qres.1997.1908.
Cooke, T., 1908. Salvia. In: Fl. Bombay, (2)1 Compositae to Gramineae. Taylor &
Francis, London, pp. 473–475.
Cordova, C.E., Lehman, P.H., 2005. Holocene environmental change in southwestern
Crimea (Ukraine) in pollen and soil records. Holocene 15, 263–277. http://dx.
doi.org/10.1191/0959683605hl791rp.
Cramer, L.H., 1981. Labiatae. In: Dassanayake, M.D. (Ed.), Fl. Ceylon., vol. 3. Amerind
Publishing Co., New Delhi, pp. 108–194.
Darriba, D., Taboada, G.L., Doallo, R., Posada, D., 2012. JModelTest 2: more models,
new heuristics and parallel computing. Nat. Methods 9, 772. http://dx.doi.org/
10.1038/nmeth.2109.
Davis, P.H., Hedge, I.C., 1971. Floristic links between NW Africa and SW Asia. Ann.
Nat. Mus. Wien 75, 43–57.
Dillenberger, M.S., Kadereit, J.W., 2014. Maximum polyphyly: multiple origins and
delimitation with plesiomorphic characters require a new circumscription of
Minuartia (Caryophyllaceae). Taxon 63, 64–88. http://dx.doi.org/10.12705/
631.5.
Dönmez, A.A., 2001. A new Turkish species of Salvia L. (Lamiaceae). Bot. J. Linn. Soc.
137, 413–416. http://dx.doi.org/10.1006/bojl.2001.0482.
Dos Santos, E.P., 1991. Genre Salvia L. sous-genre Calosphace (Benth.) Benth. section
Nobiles (Benth.) Epl. (Labiatae). Bradea 5, 436–453.
Dos Santos, E.P., 1995. Phylogenie et phytogeographie du genre Salvia L. section
Rudes (Benth.) Epl. (Lamiacees). Biogeographica 71, 15–32.
Dos Santos, E.P., 1996. Révision de la section Rudes (Benth.) Epling du genre Salvia L.
sousgenre Calosphace (Benth.) Benth. (Labiatae). Candolle 51, 19–57.
Dos Santos, E.P., Paton, A.J., Savolainen, V., 2005. Phylogeny and evolution on Salvia
subgenus Calosphace (Lamiaceae): a Brazilian view. 17. IBC. Vienna, Austria
(poster).
Drew, B.T., Sytsma, K.J., 2012. Phylogenetics, biogeography, and staminal evolution
in the tribe Mentheae (Lamiaceae). Am. J. Bot. 99, 933–953. http://dx.doi.org/
10.3732/ajb.1100549.
Drummond, A.J., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by
sampling trees. BMC Evol. Biol. 7, 214. http://dx.doi.org/10.1186/1471-2148-7214.
El-Gazzar, A., Watson, L., Williams, W.T., Lance, G.N., 1968. The taxonomy of Salvia:
a test of two radically different numerical methods. J. Linn. Soc. (Bot.) 60, 237–
250.
55
Emadzade, K., Lehnebach, C., Lockhart, P., Hörandl, E., 2010. A molecular phylogeny,
morphology and classification of genera of Ranunculeae (Ranunculaceae). Taxon
59, 809–828.
Emboden, W.A., 1964. Pollen morphology of the genus Salvia, section Audibertia.
Pollen Spores 6, 527–536.
Emboden, W.A., Lewis, H., 1967. Terpenes as taxonomic characters in Salvia section
Audibertia. Brittonia 19, 152–160.
Epling, C., 1938. The Californian salvias. A review of Salvia, section Audibertia. Ann.
Mo. Bot. Gard. 25, 95–188.
Epling, C., 1939. A Revision of Salvia, Subgenus Calosphace, vol. 10. Verl. d.
Repertoriums, Berlin.
Epling, C., Lewis, H., Raven, P.H., 1962. Chromosomes of Salvia section Audibertia.
Aliso 5, 217–221.
Espejo-Serna, A., Ramamoorthy, T.P., 1993. Revisión taxonómica de Salvia sección
Sigmoideae (Lamiaceae). Acta Bot. Mex. 23, 65–102.
Feinbrun-Dothan, N., 1978. Salvia. Fl. Palaestina, vol. 3. Isr. Acad. Sci., Jerusalem, pp.
133–145.
Fernández-Alonso, J.L., 2006. Revisión taxonómica de Salvia sect. Siphonantha
(Labiatae). An. Jard. Bot. Madrid. 63, 145–157.
Fernández Alonso, J.L., 2012. Salvia guacana, una nueva Labiatae de Colombia con
flores resupinadas y sinopsis de Salvia sect. Tubiflorae. Rev. Acad. Colomb. Cienc.
36, 517–533.
Fernández-Alonso, J.L., 2014. Salvia guaneorum (Labiatae), a new species from the
Chicamocha Canyon, Colombia. Phytotaxa 156, 221–228. http://dx.doi.org/
10.11646/phytotaxa.156.4.4.
Fragoso-Martínez, I., Martínez-Gordillo, M., 2013. Una nueava especie del género
Salvia sección Membranaceae de Guerrero, México. Acta Bot. Mex. 103, 1–9.
Fragoso-Martínez, I., Martínez-Gordillo, M., De Luna, E., 2015. Salvia semiscaposa
(Lamiaceae) a new species from Nanchititla, Mexico. Phytotaxa 219, 058–068.
http://dx.doi.org/10.11646/phytotaxa.219.1.4.
Froissart, C., 2008. La connaicance des sauges. Aix-en-Provence, France.
Fujita, Y., 1970. Evolution of chromosome numbers in the Lamiaceae, especially its
relation to the classification and phylogeny of the genus Salvia based on the
constituents of essential oils. Acta Phytotaxon. Geobot. 24, 113–121.
Geissert, F., Gregor, H.-J., Mai, D.H., 1990. Die ‘‘Saubaggerflora”, eine Frucht- und
Samenflora aus dem Grenzbereich Miozän-Pliozän von Sessenheim im Elsaß
(Frankreich). Doc. Nat. 57, 67–68.
Gladenkov, A.Y., Oleinik, A.E., Marincovich, L., Barinov, K.B., 2002. A refined age for
the earliest opening of Bering Strait. Palaeogeogr. Paleoclimatol. Palaeoecol.
183, 321–328.
González-Gallegos, J.G., 2013. Salvia albicalyx and Salvia topiensis (Lamiaceae), two
new species from Durango, Mexico. Phytotaxa 77, 9–18. http://dx.doi.org/
10.11646/phytotaxa.77.1.3.
González-Gallegos, J.G., 2014. Revision of Salvia subg. Calosphace sect.
Membranaceae (Lamiaceae). Telopea 16, 43–81. http://dx.doi.org/10.7751/
telopea20147483.
González-Gallegos, J.G., 2015. Two New Salvia Species (Lamiaceae) from the Sierra
Madre Occidental, Durango, Mexico. Syst. Bot. 40 (4). http://dx.doi.org/10.1600/
036364415X690139.
González-Gallegos, J.G., Aguilar-Santelises, Y.R., 2014. Salvia tilantongensis
(Lamiaceae), una especie nueva de la Mixteca Alta de Oaxaca, México. Acta
Bot. Mex. 109, 1–22.
González-Gallegos, J.G., Castro-Castro, A., 2012. Salvia cualensis and Salvia cualensis
var. perezii (Lamiaceae), two new taxa from the Sierra de El Cuale, Jalisco,
Mexico. Phytotaxa 74, 47–58.
González-Gallegos, J.G., Castro-Castro, A., 2013. New insights on Salvia platyphylla
(Lamiaceae) and description of S. pugana and S. albiterrarum, two new species
http://dx.doi.org/
from
Jalisco,
Mexico.
Phytotaxa,
93.
10.11646/phytotaxa.93.2.1.
Gonzáles-Gallegos, J.G., Gama-Villanueva, O.J., 2013. Resurrection of Salvia species
(Lamiaceae) recently synonymized in Flora Mesoamericana. Phytotaxa 151, 1–
24. http://dx.doi.org/10.7751/telopea20147483.
González-Gallegos, J.G., Morales-Arias, J.G., Rodríguez-Hernández, J.L., 2012a. Salvia
cacomensis (Lamiaceae), a new species from Jalisco, Mexico. Rev. Mex. Biodiv.
83, 341–346. http://dx.doi.org/10.1007/s12228-012-9297-2.
González Gallegos, J.G., Vázquez García, J.A., Cházaro Basáñez, M.J., 2013. Salvia
carreyesii, Salvia ibugana and Salvia ramirezii (Lamiaceae), three new species
from Jalisco, Mexico. Rev. Mex. Biodiv. 84, 7–19. http://dx.doi.org/10.7550/
rmb.29131.
González-Gallegos, J.G., Vázquez-García, J.A., Santana-Michel, F.J., Cuevas-Guzmán,
R., Guzmán-Hernández, L., 2012b. Salvia meera, S. rogersiana, S. santanae and S.
concolor var. iltisii (Lamiaceae), three new species and a variety from Jalisco,
Mexico. Rev. Mex. Biodiv. 83, 591–604. http://dx.doi.org/10.7550/rmb.26217.
Gray, J.T., 1872. Notes on Labiatae. Proc. Am. Acad. Arts Sci. 8, 365–372.
Greene, E.L., 1892. On certain Californian Labiatae. Pittonia 2, 301–302.
Greuter, W., Burdet, H.M., Long, G., 1986. Salvia. In: Greuter, W., Burdet, H.M., Long,
G. (Eds.), Med.-Checklist. 3, Dicotyledones (Convolvulaceae – Labiatae).
Conservatoire Jard. bot., Genève.
Haber, R.M., Semaan, M.T., 2004. Salvia fairuziana (Lamiaceae), a new species from
Lebanon. Novon 14, 437–439.
Hamazaoğlu, E., Duran, A., Pınar, N.M., 2005. Salvia anatolica (Lamiaceae), a new
species from East Anatolia, Turkey. Ann. Bot. Fenn. 42, 215–220.
Harley, R.M., Heywood, C.A., 1992. Chromosome numbers in tropical American
Labiatae. In: Harley, R.M., Reynolds, T. (Eds.), Adv. Labiate Sci.. Roy. Bot. Gard.,
Kew, pp. 211–246.
56
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Harley, R.M., Atkins, S., Budantsev, A.L., Cantino, P.D., Conn, B.J., Grayer, R., Harley,
M.M., Kok, R., Krestovskaja, T., Morales, R., Paton, A.J., Ryding, O., Upson, T.,
2004. Labiatae. In: Kadereit, J.W. (Ed.), Families and Genera of Vascular Plants,
vol. VII. Springer, Berlin Heidelberg, pp. 167–275.
Harvey, W.H., Sonder, O.W., Thiselton-Dyer, W.T., Hill, A.W., 1912. Salvia. In:
Thiselton-Dyer, W.T., Hill, A.W. (Eds.), Fl. Capensis, V Sect. I: Acanthaceae to
Proteaceae. L. Reeve, London, pp. 307–333.
Hedge, I.C., 1957. Studies in East Mediterranean species of Salvia. Notes Roy. Bot.
Gard. Edinb. 22, 173–188.
Hedge, I.C., 1959. Studies in East Mediterranean species of Salvia: II. Notes Roy. Bot.
Gard. Edinb. 23, 47–69.
Hedge, I.C., 1960. Two remarkable new Salvias from Afghanistan. Notes Roy. Bot.
Gard. Edinb. 23, 163–165.
Hedge, I.C., 1961. Studies in East Mediterranean species of Salvia: VI. Notes Roy. Bot.
Gard. Edinb. 23, 559–567.
Hedge, I.C., 1964. Salvia. In: Rechinger, K.H. (Ed.), Fl. Lowland Iraq. Verl. J. Cramer,
Weinheim, pp. 523–527.
Hedge, I.C., 1966. Studies in the flora of Afghanistan III an account of Salvia. Notes
Roy. Bot. Gard. Edinb. 26, 407–425.
Hedge, I.C., 1972a. Salvia. In: Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M.,
Valentine, D.H., Walters, S.M., Webb, D.A. (Eds.), Fl. Europaea, vol. 3. Cambridge
Univ. Press, Cambridge, pp. 188–192.
Hedge, I.C., 1972b. Salvia in Madagascar. Notes Roy. Bot. Gard. Edinb. 32, 1–11.
Hedge, I.C., 1974a. A revision of Salvia in Africa including Madagascar and the
Canary Islands. Notes Roy. Bot. Gard. Edinb. 33, 1–121.
Hedge, I.C., 1974b. A further note on Salvia tetrodonta. Notes Roy. Bot. Gard. Edinb.
33, 295–299.
Hedge, I.C., 1980. Salvia. In: Davis, P.H. (Ed.), Materials for a Flora of Turkey XXXVII.
Notes Roy. Bot. Gard. Edinb., vol. 38, pp. 47–49.
Hedge, I.C., 1982a. Salvia. In: Davis, P.H. (Ed.), Fl. Turkey, vol. 7. Edinb. Univ. Press,
Edinb, pp. 400–461. Volume.
Hedge, I.C., 1982b. Salvia. In: Rechinger, K.H. (Ed.), Fl. Iranica. Akad.. Druck- und
Verl, Graz, pp. 403–476.
Hedge, I.C., 1982c. Studies in the flora of Arabia: II Some new and interesting species
of Labiatae. Notes Roy. Bot. Gard. Edinb. 40, 63–73.
Hedge, I.C., 1985. Labiatae. In: Meikle, R.D. (Ed.), Fl. Cyprus, vol. 2. Roy. Bot. Gard.,
Kew, pp. 1287–1299.
Hedge, I.C., 1986. Labiatae of South-West Asia: diversity, distribution and
endemism. Proc. Roy. Soc. Edinb. B 89, 23–35.
Hedge, I.C., 1988. Salvia. In: Davis, P.H. (Ed.), Fl. Turkey, vol. 10. Edinb. Univ. Press,
Edinb, p. 210.
Hedge, I.C., 1992. A global survey of the biogeography of the Labiatae. In: Harley, R.
M., Reynolds, T. (Eds.), Advances in Labiate Science. Royal Bot. Gard, Kew, pp. 7–
18.
Hedge, I.C., 1998. Salvia. In: Hedge, I.C., Clement, R.A., Paton, A.J., Phillipson, P.B.
(Eds.), Fl. Madagascar, Famille 175. Labiatae. Labor de Phanérogamie, Paris, Mus.
Nat. Hist. Nat., pp. 52–94.
Hedge, I.C., 2001. Salvia. In: Davis, P.H. (Ed.), Fl. Turkey, vol. 11. Edinb. Univ. Press,
Edinb, pp. 209–210.
Hedge, I.C., Lamond, J.M., 1968. Studies in the flora of Afghanistan: VII. Notes Roy.
Bot. Gard. Edinb. 28, 89–161.
Hedge, I.C., Wendelbo, P., 1978. Patterns of distribution and endemism in Iran.
Notes Roy. Bot. Gard. Edinb. 36, 441–464.
Henderson, D.M., Prentice, H., Hedge, I.C., 1968. Pollen morphology of Salvia and
some related genera. Grana Palynol. 8, 70–85.
Hihara, S., Iwatsubo, Y., Naruhashi, N., 2001. A new natural hybrid of Salvia
(Lamiaceae) from Japan, Salvia x sakuensis. J. Phytogeogr. Taxon 49, 163–170.
Hildebrand, H., 1865. Ueber die Befruchtung der Salvia-Arten mit der Hülfe von
Insekten. Jahrb. Wiss. Bot. 4, 451–478.
Hörandl, E., 2006. Paraphyletic versus monophyletic taxa – evolutionary versus
cladistic classifications. Taxon 55, 564–570. http://dx.doi.org/10.2307/
25065631.
Hörandl, E., Paun, O., Johansson, J., Lehnebach, C., Armstrong, T., Chen, L., Lockhart,
P., 2005. Phylogenetic relationships and evolutionary traits in Ranunculus s.l.
(Ranunculaceae) inferred from ITS sequence analysis. Mol. Phylogenet. Evol. 36,
305–327. http://dx.doi.org/10.1016/j.ympev.2005.02.009.
Hörandl, E., Stuessy, T.F., 2010. Paraphyletic groups as natural units of biological
classification. Taxon 59, 1641–1653.
Hrubý, K., 1962. Key to the supraspecific taxa of the genus Salvia. Preslia 34, 368–
373.
Hu, G.-X., Liu, Y., Xu, W.-B., Liu, E.-D., 2013. Salvia petrophila sp. nov. (Lamiaceae)
from north Guangxi and south Guizhou, China. Nord. J. Bot. 32, 190–195. http://
dx.doi.org/10.1111/j.1756-1051.2013.00221.x.
Huang, T.C., Wu, J.T., 1975. A revision of Formosan Salvia. Taiwania 20, 213–228.
Huang, T.C., Wu, J.T., 1978. Labiatae. In: Li, H.L., Liu, T.S., Huang, T.C., Koyama, T., de
Vol, C.E. (Eds.), Fl. Taiwan, vol. 4. Epoch Publishing Co., Ltd., Taipei, pp. 509–519.
Ilçim, A., Celep, F., Doğan, M., 2009. Salvia marashica (Lamiaceae), a new species
from Turkey. Ann. Bot. Fenn. 46, 75–79.
Iltis, H.H., González-Gallegos, J.G., Cochrane, T.S., Vázquez-García, J.A., 2012. A new
species and a new subspecies of Salvia (Lamiaceae) from Jalisco and Michoacán,
Mexico. Brittonia 64, 343–352. http://dx.doi.org/10.1007/s12228-012-9237-1.
Jenks, A.A., Walker, J.B., Kim, S.C., 2011. Evolution and origins of the Mazatec
hallucinogenic sage, Salvia divinorum (Lamiaceae): a molecular phylogenetic
approach. J. Plant. Res. 124, 593–600. http://dx.doi.org/10.1007/s10265-0100394-6.
Jenks, A., Walker, J., Kim, S., 2013. Phylogeny of New World Salvia subgenus
Calosphace (Lamiaceae) based on cpDNA (psbA-trnH) and nrDNA (ITS) sequence
data. J. Plant. Res. 126, 483–496. http://dx.doi.org/10.1007/s10265-012-0543-1.
Jarvis, C., 2007. Order Out of Chaos. Linnaean Plant Names and their Types. Linnean
Soc. London Nat. Hist. Mus., London, UK.
Jee, V., Dhar, U., Kachroo, P., 1989. Cytogeography of some endemic taxa of Kashmir
Himalaya. Proc. Indian Nat. Sci. Acad. B: Biol. Sci. 55, 177–184.
Kadereit, J.W., Baldwin, B.G., 2012. Western Eurasian–western North American
disjunct plant taxa: the dry-adapted ends of formerly widespread north
temperate mesic lineages – and examples of long-distance dispersal. Taxon
61, 3–17.
Kahraman, A., Celep, F., Doğan, M., Bagherpour, S., 2010. A taxonomic revision of
Salvia euphratica sensu lato and its closely related species (sect. Hymenosphace,
Lamiaceae) using multivariate analysis. Turk. J. Bot. 34, 261–276.
Kahraman, A., Celep, F., Dogan, M., Guerin, G.R., Bagherpour, S., 2011a. Mericarp
morphology and its systematic implications for the genus Salvia L. section
Hymenosphace Benth. (Lamiaceae) in Turkey. Plant Syst. Evol. 292, 33–39.
http://dx.doi.org/10.1007/s00606-010-0394-y.
Kahraman, A., Doğan, M., Celep, F., 2011b. Salvia siirtica sp. nov. (Lamiaceae) from
Turkey. Nord. J. Bot. 29, 397–401. http://dx.doi.org/10.1111/j.17561051.2011.00916.x.
Kaya, A., Kutluk, H., 2007. Pollen morphology of Acinos Miller species growing in
Turkey. J. Integr. Plant Biol. 49, 1386–1392. http://dx.doi.org/10.1111/j.17447909.2007.00453.x.
King, J.E., Van Devender, T.R., 1977. Pollen analysis of fossil packrat middens from
the Sonoran Desert. Quatern. Res. 8, 191–204.
Kress, W.J., Liu, A.-Z., Newman, M., Li, Q.-J., 2005. The molecular phylogeny of Alpinia
(Zingiberaceae): a complex and polyphyletic genus of gingers. Am. J. Bot. 92,
167–178. http://dx.doi.org/10.3732/ajb.92.1.167.
Kučera, J., Košnar, J., Werner, O., 2013. Partial generic revision of Barbula (Musci:
Pottiaceae): re-establishment of Hydrogonium and Streblotrichum, and the new
genus Gymnobarbula. Taxon 62, 21–39.
Lara-Cabrera, S., Bedolla-García, B.Y., Zamudio, S., 2014. Salvia tonaticensis
(Lamiaceae), a rare new species from Mexico. Brittonia 66, 1–7. http://dx.doi.
org/10.1007/s12228-012-9297-2.
Li, X.W., Hedge, I.C., 1994. Lamiaceae. In: Wu, Z.Y., Raven, P.H. (Eds.), Fl. China, vol.
17. Sci. Press, Beijing, China & Missouri Bot. Gard., St. Louis, US, pp. 50–299.
Li, Q.Q., Li, M.H., Yuan, Q.J., Cui, Z.H., Huang, L.Q., Gen, X.P., 2013. Phylogenetic
relationships of Salvia (Lamiaceae) in China: evidence from DNA sequence
datasets. J. Syst. Evol. 51, 184–195. http://dx.doi.org/10.1111/j.17596831.2012.00232.x.
Lippert, W., 1979. Zur Kenntnis von Salvia Sektion Salvia im Westlichen
Mittelmeergebiet. Mitt. Bot. Staatssamml. München. 15, 397–423.
Mabberley, D., 2008. Mabberley’s Plant Book: A Portable Dictionary of Plants, their
Classification and Uses. Cambridge Univ. Press, New York.
Maddison, D.R., Maddison, W.P., 2000. MacClade 4.0: Analysis of Phylogeny and
Character Evolution. Sinauer Assoc., Sunderland.
Mai, D.H., 1995. Tertiäre Vegetationsgeschichte Europas: Methoden und Ergebnisse.
Gustav Fischer Verlag, Jena, Stuttgart, New York.
Mai, D.H., Majewski, J., Unger, K.P., 1963. Pliozän und Altpleistozän von Rippersroda
in Thüringen. Geologie 12, 765–815.
Mai, D.H., Walter, H., 1988. Die pliozänen Floren von Thüringen, DDR.
Quartärpalaeontology 7, 55–297.
Mansion, G., 2004. A new classification of the polyphyletic genus Centaurium Hill
(Chironiinae, Gentianaceae): description of the New World endemic Zeltnera,
and reinstatement of Gyrandra Griseb. and Schenkia Griseb. Taxon 53, 719–740.
Markova, M.L., Ivanova, P.S., 1982. Karyological study of the genus Salvia L. in
Bulgaria. Filologija 20, 3–19.
Martínez-Gordillo, M., Lozada-Pérez, L., 2011. Una nueva especie de Salvia
(Lamiaceae) de Guerrero, México. Brittonia 63, 211–214. http://dx.doi.org/
10.1007/s12228-010-9152-2.
Mercado, P., Ramamoorthy, T.P., Palomino, G., 1989. Karyotypes of five mexican
species of Salvia subgenus Calosphace (Lamiaceae). Cytologia 54, 605–608.
Merrill, E.D., 1949. Index Rafinesquianus: The Plant Names Published by C. S.
Rafinesque With Reductions, and a Consideration of His Methods, Objectives,
and Attainments. Arnold Arboretum of Harvard Univ..
Meusel, H., Jäger, E., Rauschert, S., Weinert, E., 1978. Karten. Band II. Gustav Fischer,
Jena.
Migahid, A.M., 1978. Salvia. In: Migahid, A.M. (Ed.), Fl. Saudi Arabia 1. second rev.
and illus. ed. Riyadh Univ., Riyadh, Saudi Arabia, pp. 464–465.
Miller, M.A., Pfeiffer, W., Schwartz, T., 2011. The CIPRES science gateway: a
community resource for phylogenetic analyses. In: Proceedings of the 2011
TeraGrid Conference: Extreme Digital Discovery. ACM, Salt Lake City, Utah, pp.
1–8. http://dx.doi.org/10.1145/2016741.2016785.
Milne, R.I., 2006. Northern hemisphere plant disjunction: a window on tertiary land
bridges and climate change? Ann. Bot. 98, 465–472. http://dx.doi.org/10.1093/
aob/mcl148.
Moon, H.-K., Smets, E., Huysmans, S., 2010. Phylogeny of tribe Mentheae
(Lamiaceae): the story of molecules and micromorphological characters.
Taxon 59, 1065–1076.
Mouterde, P., 1983. Salvia. In: Charpin, A., Dittrich, M. (Eds.), Nouv. Fl. Liban et Syrie.
Dar el-Machreq SARL, Beyrouth, Liban, pp. 155–171.
Müller, J., 1981. Fossil pollen records of extant angiosperms. Bot. Rev. 47, 1–142.
Neisess, K.R., 1983. Evolution, Systematics, and Terpene Relationships of Salvia
Section Audibertia (Ph.D. Thesis). Univ. of Calif., Riverside, p. 327.
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Nepokroeff, M., Bremer, B., Sytsma, K.J., 1999. Reorganization of the genus
Psychotria and tribe Psychotrieae (Rubiaceae) inferred from ITS and rbcL
sequence data. Syst. Bot. 24, 5–27. http://dx.doi.org/10.2307/2419383.
Nikitina, E.V., 1962. Salvia vvedenskii. In: Vvedenskiĭ, A.I. (Ed.), Flora Kirghiz SSR
Academy of Sciences of the Kirghiz SSR, Frunze, pp. 377–378 (in Russian).
Nowak, C.L., Nowak, R.S., Tausch, R.J., Wigand, P.E., 1994. A 30000 year record of
vegetation dynamics at a semi-arid locale in the Great Basin. J. Veg. Sci. 5, 579–
590.
Noyes, R.D., Rieseberg, L.H., 1999. ITS sequence data support a single origin for
North American Astereae (Asteraceae) and reflect deep geographic divisions in
Aster s.l. Am. J. Bot. 86, 398–412.
Ohwi, J., 1984. Fl. Japan. Smithsonian Institution, Washington, DC (in Japanese).
Osaloo, S.K., Maassoumi, A.A., Murakami, N., 2003. Molecular systematics of the
genus Astragalus L. (Fabaceae): phylogenetic analyses of nuclear ribosomal DNA
internal transcribed spacers and chloroplast gene ndhF sequences. Plant Syst.
Evol. 242, 1–32. http://dx.doi.org/10.1007/s00606-003-0014-1.
Palomino, G., Mercado, P., Ramamoorthy, T.P., 1986. Chromosomes of Salvia
subgenus Calosphace (Lamiaceae), a preliminary report. Cytologia 51, 381–386.
Peñuelas, J., Lloret, F., Montoya, R., 2001. Severe drought effects on Mediterranean
woody flora in Spain. For. Sci. 47, 214–218.
Peter, E., 1936. Revision der indischen und tibetanischen Arten der Gattung Salvia L.
Feddes Repert. Spec. Nov. Regni Veget. 39, 173–186.
Peterson, K.M., 1978. Systematic studies of Salvia L. subgenus Calosphace (Benth.)
Benth. in Benth. & Hook section Farinaceae (Epling) Epling (Lamiaceae) (Ph.D.
Thesis). Univ. of Maryland, Baltimore, p. 191.
Pobedimova, E.G., 1954. Labiatae. In: Shishkin, B.K. (Ed.), Fl. U.S.S.R., vol. XXI.
Program Sci. Translations, Jerusalem, Israel, pp. 178–260 (english translation,
1977).
Post, G.E., 1933. Fl. Syria, Palestine and Sinai. Am. Press., Beirut, pp. 347–362.
Rafinesque, C.S., 1837. Centuria VIII. In: Rafinesque, C.S. (Ed.), Synopticla Flora –
Flora Telluriana. H. Probasco, Philadelphia, pp. 83–94.
Rastipishe, S., Pakravan, M., Tavassoli, A., 2011. Phylogenetic relationships in
Ranunculus species (Ranunculaceae) based on nrDNA ITS and cpDNA trnL-F
sequences. Prog. Biol. Sci. 1, 41–47.
Reales, A., Rivera, D., Palazon, J.A., Obon, C., 2004. Numerical taxonomy study of
Salvia sect. Salvia (Labiatae). Bot. J. Linn. Soc. 145, 353–371. http://dx.doi.org/
10.1111/j.1095-8339.2004.00295.x.
Rechinger fil, K.H., 1943. Fl. Aegaea, vol. 105(1). Springer, Wien, pp. 518–522.
Rechinger, K.H., Wendelbo, P., 1967. Zhumeria, eine neue Labiaten-Gattung aus SüdIran. Nytt Mag. Bot. 14, 39–43.
Reisfield, A.S., 1987. Systematic Studies in Salvia L. (Lamiaceae) with special
emphasis on subgenus Calosphace (Benth.) Benth. section Dusenostachys Epl.
(Master thesis) Univ. of Wisconsin, Madison, p. 423.
Ronquist, F., Huelsenbeck, J.P., 2003. MrBayes 3: Bayesian phylogenetic inference
under mixed models. Bioinformatics 19, 1572–1574. http://dx.doi.org/10.1093/
bioinformatics/btg180.
Rosúa, J.L., Blanca, G., 1986. Revisión del género Salvia L. (Lamiaceae) en el
Mediterráneo Occidental: la sección Salvia. Acta Bot. Malacitana. 11, 227–271.
Rosúa, J.L., Blanca, G., 1988. Revisión del género Salvia L. sect. Aethiopis Benth.
(Lamiaceae) en el Metiterráneo Occidental. Collectanea Bot. 17, 205–236.
Sagástegui Alva, A., Rodríguez Rodríguez, E.F., 2012. Una nueva especie de Salvia
(Lamiaceae) del Norte de Perú. Rev. Peruana Biol. 19.
Saggoo, M.I., Bir, S.S., 1986. Meiotic studies on some east Himalayan members of
family Labiatae. J. Indian Bot. Soc. 65, 304–309.
Sales, F., Hedge, I.C., Christie, F., 2010. Salvia plebeia R.Br.: taxonomy,
phytogeography, autogamy and myxospermy. Pak. J. Bot. 42, 99–110.
Santos, A., Fernandez, M., 1986. Salvia herbanica spec. nova (Labiatae) en la flora de
Fuerteventura (I. Canarias). Lazaroa 9, 51–54.
Shaw, J., Lickey, E.B., Schilling, E.E., Small, R.L., 2007. Comparison of whole
chloroplast genome sequences to choose noncoding regions for phylogenetic
studies in angiosperms: the tortoise and the hare III. Am. J. Bot. 94, 275–288.
Shiuchi, T., Kanemoto, T., 2001. Chromosome numbers of plants cultivated in the
Botanic Garden of Toyama (2). Bull. Bot. Gard. Toyama 6, 47–51.
Song, Z.Q., Wang, J.H., Xie, Y.I., 2010. Karyological studies of Salvia miltiorrhiza in
China. Caryologia 63, 269–277.
Spaulding, W.G., 1983. Late Wisconsin macrofossil records of desert vegetation in
the American Southwest. Quatern. Res. 19, 256–264.
Spaulding, W.G., 1990. Vegetation dynamics during the last deglaciation,
southeastern Great Basin, U.S.A. Quatern. Res. 33, 188–203.
Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic
analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–
2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
Stamatakis, A., Hoover, P., Rougemont, J., 2008. Rapid bootstrap algorithm for the
RAxML web-servers. Syst. Biol. 75, 758–771. http://dx.doi.org/10.1080/
10635150802429642.
Stewart, R.R., 1972. Salvia. In: Nasir, E., Ali, S.I. (Eds.), Fl. West Pakistan. Fakhri
Printing Press, Karachi, pp. 630–632.
Stibal, E., 1934. Labiatae – Salvia L. (nebst Revision der chinesischen und
ostbirmanischen Arten der Gattung). Acta Hort. Gothob. 9, 101–145.
Stibal, E., 1935. Revision der Gruppe der Salvia japonica. Acta Hort. Gothob. 10, 55–
69.
Strachan, J.L., 1982. A revision of the Salvia dorrii complex (Lamiaceae). Brittonia 34,
151–169.
Strid, A., Franzen, R., 1983. Chromosome numbers in flowering plants from Greece.
Willdenowia 13, 329–333.
57
Suc, J.P., 1984. Origin and evolution of the Mediterranean vegetation and climate in
Europe. Nature 307, 429–432.
Sudarmono, H.O., 2007. Speciation process of Salvia isensis (Lamiaceae), a species
endemic to serpentine areas in the Ise-Tokai district, Japan, from the viewpoint
of the contradictory phylogenetic trees generated from chloroplast and nuclear
DNA. J. Plant. Res. 120, 483–490. http://dx.doi.org/10.1007/s10265-007-0075-2.
Sudarmono, S., Okada, H., 2008. Genetic differentiations among the populations of
Salvia japonica (Lamiaceae) and its related species. HAYATI J. Biosci. 15, 18–26.
Sun, H.T., 1977. Salvia. In: Wu, C.W., Li, H.W. (Eds.), Fl. Reip. Pop. Sin.. Sci. Press,
Beijing, pp. 70–196 (in Chinese).
Takano, A., Okada, H., 2011. Phylogenetic relationships among subgenera, species,
and varieties of Japanese Salvia L. (Lamiaceae). J. Plant. Res. 124, 245–252.
http://dx.doi.org/10.1007/s10265-010-0367-9.
Takano, A., Sera, T., Kurosaki, N., 2014. A new species of Salvia (Lamiaceae) from
Chugoku District, Japan, Salvia akiensis sp. nov. Acta Phytotax. Geobot. 65, 99–
104.
Taylor, R.M., Ayers, T.J., 2006. Systematics of Salvia pachyphylla (Lamiaceae).
Madroño 53, 11–24. http://dx.doi.org/10.3120/0024-9637(2006) 53[11:SOSPL]
2.0.CO;2.
Teodoridis, V., Kvaček, Z., Uhl, D., 2009. Pliocene palaeoenvironment and correlation
of the Sessenheim-Auenheim floristic complex (Alsace, France). Palaeodiversity
2, 1–17.
Thiébaut, J., 1953. Salvia. In: Thiébaut, J. (Ed.), Fl. Libano-Syriénne, vol. 3. C.N.R.S.,
Paris, pp. 55–62.
Thulin, M., 1993. Salvia (Labiatae) in the mountains of Northern Somalia. Opera Bot.
121, 145–148.
Thulin, M., 2009. Salvia geminata sp. nov. with remarkable stamen arrangement
from southern Yemen, with notes on S. areysiana (Lamiaceae). Nord. J. Bot. 27,
336–338. http://dx.doi.org/10.1111/j.1756-1051.2009.00538.x.
Torke, B., 2000. A revision of Salvia sect. Ekmania (Lamiaceae). Brittonia 52, 265–
302.
Torrey, J., 1859. Salvia. Botany of the Boundary, vol. 2/1. C. Wendel, Washington, p.
132.
Turner, B.L., 2011. Recension of Mexican species of Salvia sect. Stanleyana
(Lamiaceae). Phytoneuron 23, 1–6.
Turner, B.L., 2013. Taxonomic overview of the Mexican species of Salvia sect.
Flocculosae (Lamiaceae). Phytoneuron 36, 1–11.
Valiente-Banuet, A., Rumebe, A.V., Verdú, M., Callaway, R.M., 2006. Modern
Quaternary plant lineages promote diversity through facilitation of ancient
Tertiary lineages. Proc. Natl. Acad. Sci. U.S.A. 103, 16812–16817. http://dx.doi.
org/10.1073/pnas.0604933103.
Van Devender, T.R., 1987. Holocene vegetation and climate in the Puerto Blanco
Mountains, Southwestern Arizona. Quartern. Res. 27, 51–72. http://dx.doi.org/
10.1016/0033-5894(87)90049-4.
Van Jaarsveld, E.J., 1999. Salvia thermara, a new species from the Western Cape,
South Africa. Bothalia 29, 100–102.
Véliz Pérez, M.E., Quedensley, T.S., 2011. Salvia carrilloi (Lamiaceae), a new species
from Guatemala. J. Bot. Res. Inst. Tex. 5, 471–474.
Vij, S.P., Kashyap, S.K., 1975. In IOPB chromosome number reports XLVIII. Taxon 24,
367–372.
Vij, S.P., Kashyap, S.K., 1976. Cytological studies in some North Indian Labiatae.
Cytologia 41, 713–719.
Vir Jee, D.U., Kachroo, P., 1985. Chromosomal conspectus of some alpine-subalpine
taxa of Kashmir Himalaya. Chromosome Inf. Serv. 39, 33–35.
Von Hagen, V.W., 1947. Rafinesque – the unnatural Naturalist. Nat. Hist. 56, 296–
303.
Vural, M., Adigüzel, N., 1996. A new species from Central Anatolia: Salvia aytachii M.
Vural et N. Adigüzel (Labiatae). Turk. J. Bot. 20, 531–534.
Walker, J.B., Elisens, W.J., 2001. A revision of Salvia section Heterosphace
(Lamiaceae) in western North America. Sida 19, 571–589.
Walker, J.B., Sytsma, K.J., 2006. A molecular phylogenetic analysis of Salvia subgenus
Audibertia. In: Walker, J.B. (Ed.), Systematics of the Genus Salvia (Lamiaceae).
Univ. of Wisconsin-Madison, U.S, pp. 133–194 (Ph.D. Thesis).
Walker, J.B., Sytsma, K.J., 2007. Staminal evolution in the genus Salvia (Lamiaceae):
molecular phylogenetic evidence for multiple origins of the staminal lever. Ann.
Bot. 100, 375–391. http://dx.doi.org/10.1093/aob/mcl176.
Walker, J.B., Sytsma, K.J., Treutlein, J., Wink, M., 2004. Salvia (Lamiaceae) is not
monophyletic: implications for the systematics, radiation, and ecological
specializations of Salvia and tribe Mentheae. Am. J. Bot. 91, 1115–1125.
http://dx.doi.org/10.3732/ajb.91.7.1115.
Walker, J.B., Drew, B.T., Sytsma, K.J., 2015. Unravelling species relationships and
diversification within the iconic California Floristic Province sages (Salvia
Subgenus Audibertia, Lamiaceae). Syst. Bot. 40, 826–844. http://dx.doi.org/
10.1600/036364415X689285.
Wang, M., Zhang, L., Ding, C.B., Yang, R.W., Zhou, Y.H., Yang, Z.J., Yin, Z.Q., 2009.
Meiotic observations of eight taxa in the genus Salvia. Caryologia 62, 334–340.
Wang, M., Zhao, H.X., Wang, L., Wang, T., Yang, R.W., Wang, X.L., Zhou, Y.H., Ding, C.
B., Zhang, L., 2013. Potential use of DNA barcoding for the identification of Salvia
based on cpDNA and nrDNA sequences. Gene 528, 206–215. http://dx.doi.org/
10.1016/j.gene.2013.07.009.
Ward, D.E., 1984. Chromosome counts from New Mexico and Mexico. Phytologia 56,
55–60.
Weese, T.L., Bohs, L., 2007. A three-gene phylogeny of the genus Solanum
(Solanaceae).
Syst.
Bot.
32,
445–463.
http://dx.doi.org/10.1600/
036364407781179671.
58
M. Will, R. Claßen-Bockhoff / Molecular Phylogenetics and Evolution 109 (2017) 33–58
Wells, P.V., 1976. Macrofossil analysis of wood rat (Neotoma) middens as a key to
the Quaternary vegetation history of arid America. Quatern. Res. 6, 223–248.
Wen, J., 1999. Evolution of Eastern Asian and Eastern North American disjunct
distributions in flowering plants. Annu. Rev. Ecol. Syst. 30, 421–455.
Wester, P., Claßen-Bockhoff, R., 2011. Pollination syndromes of New World Salvia
species with special reference to bird pollination. Ann. Mo. Bot. Gard. 98, 101–
155. http://dx.doi.org/10.3417/2007035.
White, T.J., Bruns, T., Lee, S., Taylor, J.W., 1990. Amplification and direct sequencing
of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to
Methods and Applications. Academic Press, New York, pp. 315–322.
Whitehouse, E., 1949. Revision of Salvia section Salviastrum Gray. Field Lab. 17, 151–
165.
Whitten, W.M., Blanco, M.A., Williams, N.H., Koehler, S., Carnevali, G., Singer, R.B.,
Endara, L., Neubig, K.M., 2007. Molecular phylogenetics of Maxillaria and related
genera (Orchidaceae: Cymbidieae) based on combined molecular data sets. Am.
J. Bot. 94, 1860–1889. http://dx.doi.org/10.3732/ajb.94.11.1860.
Will, M., Claßen-Bockhoff, R., 2014. Why Africa matters: evolution of Old World
Salvia (Lamiaceae) in Africa. Ann. Bot. 114, 61–83. http://dx.doi.org/10.1093/
aob/mcu081.
Will, M., Schmalz, N., Claßen-Bockhoff, R., 2015. Towards a new classification of
Salvia s.l. – (re)establishing genus Pleudia Raf. Turk. J. Bot. 39, 693–707. http://
dx.doi.org/10.3906/bot-1405-34.
Wu, J.-T., Huang, T.-C., 1975. Biosystematic studies of Formosan Salvia. Taiwania 20,
77–98.
Xiang, Q.-Y., Soltis, D.E., Soltis, P.S., Manchester, S.R., Crawford, D.J., 2000. Timing the
Eastern Asian-Eastern North American floristic disjunction: molecular clock
corroborates paleontological estimates. Mol. Phylogenet. Evol. 15, 462–472.
http://dx.doi.org/10.1006/mpev.2000.0766.
Yang, Z., Xun, G., Yuezhi, P., 2004. Cytological study of six Salvia species (Lamiaceae)
from the Hengduanshan Mountains region of China. Caryologia 57, 360–366.
Yang, Z., Zhang, L., Zhao, H., Yang, R., Ding, C., Zhou, Y., Wan, D., 2009. Chromosome
numbers of some species of Salvia (Lamicaeae) from Sichuan Province, China.
Nord. J. Bot. 27, 287–291. http://dx.doi.org/10.1111/j.1756-1051.2009.00376.x.
Yıldırımlı, S
ß ., Ertekin, A.S., 2008. Salvia ertekinii Yıldırımlı, sp. nov. Sistematik Bot.
Dergisi- Herb J. Syst. Bot. 15, 5–8.
Zander, R.H., 2008. Evolutionary inferences from non-monophyly on molecular
trees. Taxon 57, 1182–1188.
Zhao, H., Zhang, L., Fan, X., Yang, R., Ding, C., Zhou, Y., 2006. Studies on chromosome
numbers of Salvia miltiorrhiza, S. flava and S. evansiana. China J. Chin. Mater.
Med. 31, 1847–1849. http://dx.doi.org/10.3417/1055-3177(2007) 17[206:
TNSISS]2.0.CO;2.
Zhu, Z.-Y., Min, B.-Q., Wang, Q.-L., 2011. Taxa nova Salviorum labiatarum. Bull. Bot.
Res. 31, 1–3. http://dx.doi.org/10.7525/j.issn.1673-5102.2011.01.001.
Zimmermann, N.F.A., Ritz, C.M., Hellwig, F.H., 2010. Further support for the
phylogenetic relationships within Euphorbia L. (Euphorbiaceae) from nrITS
and trnL-trnF IGS sequence data. Plant Syst. Evol. 286, 39–58. http://dx.doi.org/
10.1007/s00606-010-0272-7.
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