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. 2014 Jul;114(1):61–83. doi: 10.1093/aob/mcu081

Why Africa matters: evolution of Old World Salvia (Lamiaceae) in Africa

Maria Will 1,*, Regine Claßen-Bockhoff 1
PMCID: PMC4071099  PMID: 24966353

Abstract

Background and Aims

Salvia is the largest genus in Lamiaceae and it has recently been found to be non-monophyletic. Molecular data on Old World Salvia are largely lacking. In this study, we present data concerning Salvia in Africa. The focus is on the colonization of the continent, character evolution and the switch of pollination systems in the genus.

Methods

Maximum likelihood and Bayesian inference were used for phylogenetic reconstruction. Analyses were based on two nuclear markers [internal transcribed spacer (ITS) and external transcribed spacer (ETS)] and one plastid marker (rpl32-trnL). Sequence data were generated for 41 of the 62 African taxa (66 %). Mesquite was used to reconstruct ancestral character states for distribution, life form, calyx shape, stamen type and pollination syndrome.

Key Results

Salvia in Africa is non-monophyletic. Each of the five major regions in Africa, except Madagascar, was colonized at least twice, and floristic links between North African, south-west Asian and European species are strongly supported. The large radiation in Sub-Saharan Africa (23 species) can be traced back to dispersal from North Africa via East Africa to the Cape Region. Adaptation to bird pollination in southern Africa and Madagascar reflects parallel evolution.

Conclusions

The phenotypic diversity in African Salvia is associated with repeated introductions to the continent. Many important evolutionary processes, such as colonization, adaptation, parallelism and character transformation, are reflected in this comparatively small group. The data presented in this study can help to understand the evolution of Salvia sensu lato and other large genera.

Keywords: Salvia, Lamiaceae, Canary Islands, character evolution, ITS, ETS, Madagascar, ornithophily, pollination, rpl32-trnL, Sub-Saharan Africa

INTRODUCTION

Throughout the world, many Salvia spp. (Lamiaceae) are known as ornamental (e.g. S. coccinea, S. patens, S. viridis), medicinal (S. officinalis, S. miltiorhiza) and even hallucinogenic plants (S. divinorum) (Clebsch, 2008; Froissart, 2008). Salvia is the largest genus in the mint family, with 900–1000 species distributed worldwide (Alziar, 1988–1993; Harley et al., 2004). Molecular studies have shown many large genera to be non-monophyletic, and this is also true for Salvia (Walker et al., 2004), with respect to Dorystaechas, Meriandra, Perovskia, Rosmarinus and Zhumeria (Walker and Sytsma, 2007). Major clades containing Salvia spp. were named Salvia Clade I, II and ‘III’ Salvia (s.l.). So far, previous molecular studies have focused on New World (NW) Salvia. In contrast, Old World (OW) species have been largely disregarded (Walker et al., 2004; Sudarmono, 2007, 2008; Walker and Sytsma, 2007; Jenks et al., 2011, 2012; Li et al., 2013). Only seven African species were included in the genus-wide study of Walker and Sytsma (2007), which revealed that they are members of two of the three major clades proposed by the authors (Fig. 1; Clade I, ‘Clade III’). In this study, Salvia ‘Clade III’ is paraphyletic with respect to Zhumeria majdae. Thus, we accept the south-west (SW) Asian species and Zhumeria as one clade (S. trichocalycina group; Clade III) and the East Asian species as the fourth independent evolutionary lineage (S. miltiorhiza group; Clade IV). According to Walker and Sytsma (2007), Salvia Clade I is monophyletic and covers the type species of the genus (S. officinalis; Jarvis, 2007). We therefore refer to it as Salvia sensu stricto (s.s.).

Fig. 1.

Fig. 1.

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Phylogenetic tree of Salvia s.l. defining the major clades (Walker and Sytsma, 2007, simplified, i.e. nodes with bootstrap values <75 % were collapsed). Strict consensus tree based on the combined analysis of trnL-F and ITS data; MP. Non-Salvia genera are highlighted (bold); NW Salvia is highlighted in light grey and OW taxa in dark grey. Numbers in parentheses, separated by slashes, indicate the number of African species and the total number of taxa in the corresponding clade in their analyses.

Sixty-two Salvia spp. occur in Africa and adjacent areas (Fig. 2; Hedge, 1974; Santos and Fernández, 1986; Van Jaarsveld, 1999). Most are endemics distributed in North Africa (25 species including the Canary Island endemics), southern Africa (23 species), Madagascar (six species), East Africa and on the Arabian Peninsula (eight species). Similar distribution ranges are known for other plant genera such as Androcymbium, Senecio and Zygophyllum (Caujapé-Castells, 2001; Colemann et al., 2003; Bellstedt et al., 2008; Del Hoyo et al., 2009) and for animals, e.g. Diptera (Kirk-Spriggs and McGregor, 2009). Salvia thus appears to be another genus adapted to the similar climatic conditions occurring in North (Mediterranean area), East (East African mountains) and southern (Cape Region) Africa.

Fig. 2.

Fig. 2.

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Distribution of Salvia s.l. on the African continent. Five regions on the continent and adjacent areas are recognized with 62 Salvia spp.: (1) the Canary Islands; (2) southern Europe/North Africa to south-west Asia; (3) East Africa/Arabian Peninsula; (4) southern Africa; and (5) Madagascar. Distributions are based on: Hedge (1974), Codd (1985), Santos and Fernández (1986), Thulin (1993, 2009) and Van Jaarsveld (1999).

African Salvia is of special interest for addressing evolutionary questions. Species are highly diverse in habitat preferences (Fig. 3), floral morphology (shape, size, colour and stamen construction) and pollination (Fig. 4). The only bird-pollinated species known from the Old World evolved in Sub-Saharan Africa (SSA) (Scott-Elliot, 1890; Van Jaarsveld, 1999; Wester and Claßen-Bockhoff, 2006, 2007). The most recent classification of African Salvia was presented by Hedge (1974). Based on distribution and morphology, he arranged 59 species in 23 species groups. However, it is not known to which degree these species groups represent natural lineages.

Fig. 3.

Fig. 3.

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Habitat diversity of Salvia s.l. in Africa. (A) Salvia sclarea, Anatolian steppe; (B) S. viridis, Anatolia; (C) S. thermarum, fynbos Western Cape, South Africa; (D, E) S. broussonetii, basalt maritime cliffs on Tenerife (D, dotted circles), flowering plant (E); (F) S. leucodermis, Madagascar; (G) S. herbanica, rocky habitat south-east Fuerteventura, Canary Islands; (H) S. africana-lutea, coastal sand dunes in the Western Cape; (I) S. aegyptiaca, semi-arid habitat on Gran Canaria, Canary Islands. Photographs: (A, B) F. Celep, (C, H) P. Wester, (D, E, G) R. Claßen-Bockhoff, (F) B. Bytebier, and (I) M. Thulin.

Fig. 4.

Fig. 4.

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Phenotypic diversity of Salvia s.l. in Africa. (A) Salvia verticillata; (B) S. nilotica; (C) S. disermas; (D) S. argentea; (E) S. aegyptiaca; (F) S. canariensis; (G) S. broussonetii; (H) S. herbanica; (I) S. lanceolata with Cinnyris chalybeus (southern double-collared sunbird; formerly Nectarinia chalybeus); (J) S. geminata; (K) S. taraxacifolia; (L) S. interrupta; (M) S. dolomitica; (N) S. chamelaeagnea with Xylocopa caffra (carpenter bee); (O) S. scabra; (P) S. leucodermis; (Q) S. sessilifolia; (R) S. thermarum; and (S) S. africana-lutea. Note the typical falcate upper corolla lip in bee-pollinated species (e.g. S. argentea, D) in contrast to the straight upper lip in bird-pollinated taxa (I, P–R) and the diverse floral morphologies in the Canary Islands endemics (F–H). Photographs: (A, B, C, D, F, L) M. Will, (E, H) R. Claßen-Bockhoff, (G, K, O, R, S) P. Wester, (I) R. Groneberg, (J) M. Thulin, (N) H. Technau, (P) P. B. Phillipson and (Q) D. Hannon.

In the present study, we examine the monophyly of Hedge's (1974) species groups based on a phylogenetic analysis that includes two-thirds of the African species. We intend to determine the number of independent origins of African Salvia. Furthermore, the colonization of the African continent and the evolution of African Salvia, e.g. the origin of bird pollination, are reconstructed.

MATERIALS AND METHODS

Plant material

Our analyses include 84 Salvia spp., 46 of them sequenced for the first time. We cover 41 (66 %) of the 62 African species: two endemics from Madagascar, all endemics from the Canary Islands, eight species from eastern Africa and the Arabian Peninsula, 18 southern African species and 12 species restricted to North Africa, the circum-Mediterranean area and SW Asia. Accessions derived from GenBank were used to complement the data set. Voucher information and GenBank accession numbers are provided in the Appendix. Due to the lack of suitable plant material and/or successful PCR, some species are only represented by a sub-set of the three molecular markers.

Our sampling covers all major lineages previously identified in Salvia (Walker and Sytsma, 2007; Fig. 1). Well-supported clades that are not the focus of this study (Clades II and IV; see Walker and Sytsma, 2007; Will, 2013) are represented by a sub-set of species only. Independent accessions are included, especially for taxonomically critical and polymorphic species. Hyptis laniflora was used as the outgroup in all analyses. Nomenclature is in accordance with Alziar (1988–1993) and with the International Plant Names Index (http://www.ipni.org/ipni/, accessed 30 April 2013). The term Sub-Saharan Africa is used in the sense of Linder (2001) but additionally includes the Namib–Kalahari region.

DNA extraction, amplification and sequencing

For Salvia, new sequence data are presented for the internal transcribed spacer (ITS; 39 species), the external transcribed spacer (ETS; 38 species) and the plastid marker rpl32-trnLUGA (57 species). The latter was selected based on the results of previous primer screening (trnL-F and rpl32-ndhF). Total genomic DNA was obtained from silica-dried or herbarium leaf material. DNA was extracted according to the manufacturer's protocol for the NucleoSpin® plant DNA extraction kit (Macherey-Nagel, Düren, Germany). The standard 25 μL PCR mix consisted of 2 mm MgCl2, 200 μm dNTPs, 1 pm primer, 0·025 U μL–1 Taq polymerase and 0·5–1·0 μL of DNA extract in the reaction buffer provided by the manufacturer of the polymerase.

The PCRs were carried out in a Biometra T3 or a PTC 100 MJ Research thermocycler using the following program: 60 s at 94 °C; followed by 35 cycles of 20 s at 94 °C, 30 s at 55 °C and 60 s at 72 °C; and a post-treatment of 80 s at 55 °C and 8 min at 72 °C for each marker. The whole ITS region was sequenced as a single piece using the ITS-A (Noyes and Rieseberg, 1999) and ITS-4 primers (White et al., 1990). The ETS region was sequenced using 18S-E (Baldwin and Markos, 1998) and ETS-B (Beardsley and Olmstead, 2002). For plastid sequences, we used the rpl32 and trnLUGA primers (Shaw et al., 2007). PCR products were purified according to the manufacturers' protocols using ExoSAP-IT PCR Product Clean-up (Affymetrix UK Ltd, Wooburn Green, UK) or NucleoSpin®Extract II-kit (Macherey-Nagel).

Cycle sequencing was performed using ABI Prism Big DyeReady Reaction Mix (Perkin Elmer/Applied Biosystems, Foster City, CA, USA) using the primers listed above and following the manufacturer's protocol. Products were purified with Sephadex™ G50 (VWR International GmbH, Darmstadt, Germany) and sequenced on a 16-capillary ABI 3130 xl automated sequencer (Life Technologies GmbH, Darmstadt, Germany).

DNA sequence alignment and phylogenetic analyses

Sequencing was straightforward for each marker. Forward and reverse sequences were edited manually, merged into consensus sequences using Sequencer™ 4.1.2. (GeneCodeCorp., Ann Arbor, MI, USA) and aligned manually in McClade4.1 (Maddison and Maddison, 2000). Ambiguously alignable regions (identified manually) were excluded from analyses. The three data sets were analysed separately. In order to increase resolution, we combined nuclear and plastid data (combined data set). Partitions were defined for the combined data set before the best-fit models of nucleotide substitution were selected with jModeltest 2.1.1 (Darriba et al., 2012). Under the Akaike information criterion (AIC), the GTR+I+G model was selected for the ITS data set and TVM+G for ETS and the plastid marker. Two tree searches, one under maximum likelihood (ML) with bootstrapping (BS; RAxML-HPC BlackBox v.7.4.4; Stamatakis, 2006; Stamatakis et al., 2008) and one under Bayesian inference (BI; MrBayes v.3.1.2 on XSEDE; Ronquist and Huelsenbeck, 2003), were performed on the CIPRES Science Gateway v.3.3 server (Miller et al., 2010). Since MrBayes does not allow nst = 5, required for TVM+G, we chose the more complex model (nst = 6). For BI, we ran four Markov chains simultaneously for 10 million generations analysing the plastid and ETS data sets. Two independent runs of 40 million generations were performed for the ITS and combined data sets. Every thousandth generation was sampled. The burn-in was determined with Tracer v.1.5 implemented in BEAST. We generated 50 % majority rule consensus trees with posterior probabilities (PPs) using MrBayes v.3.1.2.

The ITS, ETS and plastid data were analysed separately to identify incongruences. To combine data without conflict, strongly supported (PP = 1·00 or ≥92 % ML BS) incongruences were dealt with by the duplication of the corresponding individuals, with one duplicate having only ITS and ETS sequences, and one only having plastid sequences (Pirie et al., 2008). The absent sequences were coded as missing data (‘?’). Sequences from the same or different species that were completely identical were reduced to one haplotype. In the text or figures, sequence identity is indicated by a slash separating the corresponding accessions. The existing concept of clades sensu Walker and Sytsma (2007) was adopted, except for ‘Clade III’. The latter was split into two independent clades, i.e. the S. trichocalycina group (Clade III) and the S. miltiorrhiza group (Clade IV) (Fig. 1).

Ancestral character state reconstruction

Ancestral character states were reconstructed using the Mesquite software package v.2.75 with Fitch parsimony optimization (Maddison and Maddison, 2011). Five characters, i.e. distribution area, life form, calyx morphology, stamen type and pollination system, were coded (Supplementary Data Table S1). Character states are based on literature research and observations. Stamen classification is based on stamen types and intermediate forms introduced by Hedge (1974, 1982): A, lower lever arm with fertile thecae; B, lower lever arm sterile; and C, lower lever arm reduced. Information on pollinators is based on the literature or personal communications, or was postulated according to character syndromes (e.g. Wester and Claßen-Bockhoff, 2011). In all cases, reconstructions are performed on 100 randomly sampled trees with branch lengths from the BI analyses, as well as the consensus tree (50 % majority rule) of the combined data BI analysis (Pirie et al., 2009). Statistical support was calculated under maximum parsimony (MP).

RESULTS

Phylogenetic analyses: nrITS (Fig. 5)

Fig. 5.

Fig. 5.

Fig. 5.

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Analyses of the nrITS data set. Non-Salvia genera are highlighted (bold); names of accessions with identical sequences are separated by slashes; only support values ≥75 % (BS) and ≥0·95 (PP) are illustrated. Species distribution is indicated by different colours.

The aligned length of the nuclear data set is 637 bp, 255 (40 %) of which are potentially parsimony informative. Hyptis laniflora is found in a polytomy with (1) Collinsonia and Perilla and (2) an unresolved, weakly supported clade. Within the last of these, nine lineages are strongly supported by BI: (1) Horminum; (2) Melissa; (3) Lepechinia; (4) Perovskia; (5) Rosmarinus; (6) Clade IV; (7) Clade III plus the genus Zhumeria; (8) a trichotomy including Meriandra, Dorystaechas and NW Salvia species (Clade II); and (9) Clade I (Salvia s.s.).

Clade IV is a well-supported clade including four East Asian and one European species (S. glutinosa). Clade III consists of a trichotomy composed of (1) S. trichocalycina, (2) S. aristata and (3) S. aegyptiaca plus S. herbanica. The American Clade II is strongly supported as part of a trichotomy with the two OW genera Meriandra and Dorystaechas. It is divided into two sub-clades, with S. chionopeplica and S. cf. chionopeplica in separate sub-clades. Clade I is only supported by BI (PP = 0·99). Sub-clade I-C forms a polytomy with Clade I-A, S. judaica and S. taraxacifolia. Sub-clade I-D is sister to this clade, and the American sub-clade I-B is in turn sister to the remainder of Clade I. Within sub-clade I-D (seven species), S. cabulica is sister to a polytomy consisting of six lineages (Fig. 5: I-D). The two accessions of S. fruticosa do not cluster together. Six major lineages are recognized within sub-clade I-C. One lineage contains the two Canary Island endemics S. broussonetii and S. canariensis (Fig. 5: I-C; green). A second lineage includes the South African endemics S. radula and S. disermas (Fig. 5: I-C; magenta) along with four European species (Fig. 5: I-C; beige; monophyly for each of these species is not confirmed). Sub-clade I-A is only poorly resolved. It includes exclusively African taxa restricted to SSA. Within sub-clade I-A, one strongly supported clade includes all six Madagascan accessions (2 spp.) (Fig. 5: I-A; pink). The ML analysis weakly indicates that S. sessilifolia is paraphyletic with respect to S. leucodermis. Sequences of S. leucodermis and S. sessilifolia differ only in one position (A or C) which is ambiguous (IUPAC code: M) in S. sessilifolia accession DQ667282.

ETS (Supplementary Data Fig. S1)

The alignment contains 69 accessions (53 species), 60 (44 species) representing the genus Salvia. The aligned length of the data set is 466 bp, 230 (40·4 %) of which are potentially parsimony informative. There are few major conflicts with the ITS topology. Differences concern a clade which is moderately supported by BI (PP = 0·98) including: (1) Clade II plus Meriandra and Dorystaechas; (2) Clade III without S. aristata (here called Clade III-A); (3) Zhumeria plus S. aristata; and (4) S. przewalskii (Clade IV represented by only one species in this data set). This clade is not supported (but also not contradicted) in the ITS analyses. The incongruence between the ITS and ETS data sets is in the position of Zhumeria. However, this difference might be based on the slightly different sampling in Clade III. Furthermore, support for a monophyletic Clade II is lacking. Instead, the three lineages of NW Salvia spp. form a polytomy with Meriandra and Dorystaechas (Supplementary Data Fig. S1].

Compared with the ITS data set, support for Clade I (Salvia s.s.) is low (PP = 0·96). The four sub-clades (sub-clades I-A through I-D) form a polytomy. Differences in the topology of sub-clade I-C are mainly based on additional accessions in the ETS data set, e.g. S. canariensis 464. The latter renders S. canariensis paraphyletic with respect to S. broussonetii, but this relationship is not strongly supported. Similarly, adding S. disermas 454 causes S. disermas to be paraphyletic with respect to S. radula. Sub-clade I-A is better resolved in the ETS than in the ITS data set. The former supports sister relationships for (1) S. cf. repens 437 and S. stenophylla and (2) S. aurita and S. dolomitica. Furthermore, S. africana-caerulea, S. albicaulis, S. chamelaeagnea and S. lanceolata × africana-caerulea appear in a moderately supported clade not supported in ITS data (PP = 0·98).

rpl32-trnL (Fig. 6)

Fig. 6.

Fig. 6.

Fig. 6.

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Analyses of the rpl32-trnL data set. Non-Salvia genera are highlighted (bold); only support values ≥75 % (BS) and ≥0·95 (PP) are illustrated. Species distribution is indicated by different colours.

The aligned length of the plastid data set is 929 bp, with 246 (26·5 %) potentially informative nucleotide positions. Hyptis is again found in a trichotomy with Collinsonia and a strongly supported clade that includes all other accessions. The latter splits into two major lineages one only including non-Salvia samples (Horminum, Glechoma, Thymus, Clinopodium and Mentha). The second clade contains all Salvia samples and six additional genera. Melissa and Lepechinia are moderately supported (ML) as sister genera. They are found in a polytomy with two strongly supported clades.

The first includes Clade IV, sub-clades III-A, III-B, Zhumeria, Clade II and Dorystaechas, as found in the ETS data set. The position of Zhumeria differs from the ETS data; the genus is placed in a trichotomy with S. aristata (III-B) and the S. aegyptiaca group (III-A) based on plastid data. As in the ETS data set, the monophyly of Clade II is not supported. Instead, three sub-clades (II-A, II-B and II-C) are found in a polytomy with Dorystaechas. The most striking incongruence between nuclear and plastid data is the position of S. deserti (Fig. 6; III-A). It is sister to S. aegyptiaca based on ETS data (Supplementary Data Fig. S1) but strongly supported in a sister relationship to all species nesting in sub-clade III-A based on the plastid data set (Fig. 6). In the ITS data set, S. deserti is not represented.

The second major clade consists of a trichotomy composed of Rosmarinus, Perovskia and a strongly supported Clade I (Salvia s.s.). Compared with nuclear data, the latter is better resolved, splitting into three major lineages (sub-clades): (1) I-D (topology corresponding to nuclear data); (2) I-C; and (3) I-B plus I-A. Within sub-clade I-C, neither S. sclarea (244 and JQ669373) nor S. palaestina (400 and 200) is supported as monophyletic. Sister grouping of sub-clades I-A (Africa) and I-B (America) is in conflict with ITS data (Fig. 5). Sub-clade I-A was strongly supported by the nuclear data, but the relationships among its species were largely unresolved. However, its topology slightly differs. Instead of being part of a basal polytomy, S. chamelaeagnea 52 and S. africana-caerulea 230 are sister species in the plastid data set, closely related to S. aurita and S. scabra. The ITS data do not suggest any relationships for S. aurita, whereas the ETS data weakly support a sister relationship to S. dolomitica. Furthermore, in contrast to the ITS topology, different accessions of S. namaensis (78 and 435) and S. lanceolata (264 and 58) are not supported to be monophyletic based on plastid data.

Combined analyses of the nuclear and plastid data sets (Fig. 7)

Fig. 7.

Fig. 7.

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Analyses of the combined data set. Non-Salvia genera are highlighted (bold); GenBank accessions are marked with an asterisk (*); for taxa with only one or two markers, the corresponding marker is given after the taxon name and extraction number. Uncapitalized letters (m, f) indicate taxa described after the revision of African Salvia (Hedge, 1974); classification in the corresponding species group is based on morphology and the corresponding species description (Santos and Fernández, 1986; Thulin, 1993, 2009; Van Jaarsveld, 1999). For detailed information about ancestral character reconstruction see also Supplementary Data Table S1 and Figs S2–S6.

The aligned length of the combined data set is 1982bp, of which 582 (29·4 %) are potentially parsimony informative. The sequence duplication approach was not suitable to resolve the conflicting placement of sub-clade I-B within Salvia s.s., which was placed either at the base of Clade I (ITS; Fig. 5) or as sister to sub-clade I-A (plastid; Fig. 6). Thus, we used the tree with the best topology for illustration, being aware of the unresolved conflict for the two clades.

The combined tree largely reflects the topology of the plastid data set (e.g. sister relationship of sub-clade I-A and I-B), but shows better resolution and higher support within sub-clade I-A. Melissa is in a trichotomy with two clades containing Salvia spp. The first covers (1) Clade II, Dorystaechas and Meriandra, and the latter two moderately supported as sister; (2) sub-clades III-A, III-B and Zhumeria; and (3) Clade IV. The second includes Perovskia, Rosmarinus, and Salvia s.s. (Clade I). The latter is strongly supported and falls into the same three major lineages as in the plastid data set. As to sub-clade I-A, S. taraxacifolia is sister to all remaining taxa. Salvia nilotica splits next, followed by S. somalensis, which is sister to a large clade including only taxa from southern Africa and Madagascar. Monophyly of S. namaensis, S. repens, S. sessilifolia and S. leucodermis, each of which was represented by more than one accession, is not confirmed.

Ancestral character state reconstruction (Supplementary Data Figs S2–S6; Fig. 7)

All African areas, except Madagascar, were colonized more than once (Supplementary Data Fig. S2). The ancestral area is reconstructed as East Africa and the Arabian Peninsula for sub-clades of Salvia sensu lato (s.l.) (III-A; MP 100 %) and Salvia s.s. (sub-clade of I-C covering S. sclarea, S. schimperi, S. merjamie, S. disermas and S. radula; MP 89 %). Within the latter, S. disermas and S. radula point to the colonization (migration and/or dispersal) of southern Africa. A second colonization is supported for the largest lineage of sub-clade I-A, which only contains accessions from southern Africa (MP 94 %). Madagascar was most probably colonized from southern Africa (MP 64 %).

Reconstruction of the ancestral life form (Supplementary Data Fig. S3) revealed that three of the four defined growth forms evolved several times in parallel. Only some crown groups can clearly be characterized by this character, e.g. Clade IV (MP 100 %: perennial herbs), Clade III-A (MP 100 %; dwarf shrubs) and the clade consisting of S. canariensis and S. broussonetii (sub-clade I-C; MP 100 %; shrubs). For the clade containing Clades II, III and IV, herbaceous growth most probably reflects the ancestral state (MP 72 %). Clade IV includes exclusively herbaceous perennials, while its sister group is characterized by shrubby growth (MP 94 %). Within this clade, dwarf shrubby growth is a synapomorphy for sub-clade III-A (Fig. 7). A character transformation from herbaceous to shrubby growth is also found in Salvia s.s. (sub-clade I-A), and a reversal back to herbaceous growth is found for S. repens and S. stenophylla nesting within the same clade. Clade II (including Dorystaechas hastata and Meriandra bengalensis) appears to be originally shrubby. However, our study underrepresents the diversity of growth forms in this large NW clade, which includes shrubs, perennials, annuals and trees. The SW Asian species (sub-clade III-A, S. aristata and Zhumeria) show two different trends, one towards a suffruticose life form (S. aristata) and one towards dwarf shrubby growth (III-A).

A thick-textured, non-expanding calyx represents the ancestral state in each of the major Salvia clades (MP 100 %) (Supplementary Data Fig. S4). Expanding calyxes with widely diverging lips, which are papery and often coloured, evolved several times in parallel, not only in Salvia (sub-clades I-A, I-C and I-D) but also in Zhumeria (Fig. 7).

For stamen construction, type A with a fertile theca at the lower lever arm is strongly supported as the ancestral state in sub-clade III-A and Salvia s.s. (Supplementary Data Fig. S5). Within the latter, stamen type B evolved in sub-clade I-C and in I-A. Furthermore stamen type C is found in S. namaensis in sub-clade I-A (Fig. 7). The same reduction of the lower lever arm is found in Rosmarinus officinalis, which is not closely related to S. namaensis.

Melittophily, bee pollination, is reconstructed as the ancestral pollination system for each clade, except for sub-clade I-B (Supplementary Data Fig. S6). The latter is represented by only two species, one of them assumed to be ornithophilous and the other psychophilous (Wester and Claßen-Bockhoff, 2011). Thus, its ancestral character state remains ambiguous. Bird-pollinated flowers evolved repeatedly in the NW (Clade II and sub-clade I-B) and in the OW sub-clade I-A (Fig. 7). Within the latter, at least two pollinator shifts are suggested (Supplementary Data Fig. S6; Fig. 7), one by the Madagascan sub-clade and another by two South African species forming a clade (S. lanceolata and S. africana-lutea). A third switch to bird pollination might be represented by S. thermarum from South Africa. Two of the sampled accessions are found in a derived position of a melittophilous lineage (MP 60 %; Fig. 7).

DISCUSSION

Our study confirms the non-monophyly of both Salvia s.l. and the African Salvia spp. (Walker et al., 2004). We also confirm that all African species are restricted to two of the four major lineages of Salvia (Clades I and III; Fig. 7).

Interspecific relationships in African Salvia: species groups sensu Hedge

Subgeneric classification of the genus is based on morphology and distribution (Bentham, 1832–1836, 1848, 1876; Briquet, 1897). Hedge (1974) established 23 ‘species groups’ to address relationships among African Salvia spp. and their affinities beyond the continent. For four of these groups, molecular data can be used to discuss their monophyly.

The two taxa placed in species group V (S. disermas and S. radula) form a clade within sub-clade I-C (Fig. 7). Both species occur in southern Africa but do not overlap in their distribution (Fig. 9E: 26, 34). They have similar flower morphology but differ in flowering time and indumentum (Hedge, 1974). We confirm monophyly of this group and, based on ETS and combined data sets, find some support for Hedge's (1974) idea that S. radula could be a subspecies of S. disermas (Supplementary Data Table S1).

Fig. 9.

Fig. 9.

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Distribution of African Salvia spp. (except North Africa and circum-Mediterranean area). (A) Madagascar: (1) S. cryptoclada; (2) S. leucodermis; (3) S. parvifolia; (4) S. perrieri; (5) S. porphyrocalyx; (6) S. sessilifolia. (B) Canary Islands: (7) S. broussonetii; (8) S. canariensis; (9) S. herbanica; (10) S. aegyptiaca; (11) S. verbenaca. (C, D) East Africa and Arabian Peninsula: (12) S. areysiana; (13, black asterisk) S. bariensis; (14) S. deserti; (15) S. geminata; (16) S. merjamie; (17) S. nilotica; (18) S. schimperi; (19) S. somalensis. (E–G) southern Africa: (20) S. africana-caerulea; (21) S. africana-lutea; (22) S. albicaulis; (23) S. aurita; (24) S. chamelaeagnea; (25) S. dentata; (26) S. disermas; (27) S. dolomitica; (28) S. garipensis; (29, black asterisk) S. granitica; (30) S. lanceolata; (31) S. muirii; (32) S. namaensis; (33) S. obtusata; (34) S. radula; (35) S. repens; (36) S. runcinata; (37) S. scabra; (38) S. schlechteri; (39) S. stenophylla; (40, white asterisk) S. thermarum; (41) S. triangularis; (42) S. tysonii. Based on Codd (1985), Hedge (1974), Santos and Fernández (1986), Thulin (1993, 2009) and Van Jaarsveld (1999). Note the overlapping distributions of species in southern Africa (Fig. 7E–G) and the disjunct area of S. stenophylla (39) and S. disermas (26).

Species group F originally included three African species (Hedge, 1974). The two species included in this study (S. aegyptiaca and S. deserti) form a clade with four more recently described species (Fig. 7; III-A), all of which are adapted to arid or semi-arid habitats. Except for the widespread S. aegyptiaca (Fig. 10C: 10), they are all local endemics, e.g. in East Africa and the Arabian Peninsula (S. areysiana, S. bariensis and S. geminata) or Fuerteventura (S. herbanica) (Fig. 9B: 9; C: 12, 13, 15, D: 14). As the clade is well supported by synapomorphies, e.g. growth as dwarf shrubs with simple, revolute leaves, straight upper corolla lips with exposed stamens and minute flowers (Hedge, 1974; Santos and Fernández, 1986; Scholz, 1993; Thulin, 1993, 2009), we not only confirm monophyly of species group F but extend it to include at least the six sampled species. Based on the unique character syndrome, more species are likely to be included in this species group (Bokhari and Hedge, 1977; M. Will and R. Claßen-Bockhoff, unpubl. data). Furthermore, our data confirm the close relationship proposed for African and SW Asian Salvia (Davis and Hedge, 1971; Hedge, 1974).

Fig. 10.

Fig. 10.

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Distribution of Salvia spp. from North Africa and the circum-Mediterranean area. (A–C) (10) S. aegyptiaca; (11) S. verbenaca; (43) S. argentea; (44) S. barrelieri; (45) S. fruticosa; (46) S. lavandulifolia; (47) S. phlomoides; (48) S. sclarea; (49) S. spinosa; (50) S. viridis; (51) S. algeriensis; (52) S. balansae; (53) S. chudaei; (54) S. dominica; (55) S. gattefossei; (56) S. interrupta; (57) S. jaminiana; (58) S. lanigera; (59) S. mouretii; (60) S. palaestina; (61) S. pseudojaminiana; (62) S. taraxacifolia. Based on Hedge (1974); the distribution of S. sclarea on the Iberian Peninsula is based on Rosúa and Blanca (1986). Note the overlapping distribution of S. phlomoides (47) and S. candelabrum (endemic to the Iberian Peninsula, indicated by ‘x’; based on Rosúa and Blanca (1986).

In contrast, relationships for the monospecific species groups H and N were not predicted before. While Hedge (1974) supposed that the allies of S. canariensis (H) occur in southern Africa, he described S. broussonetii (N) as a relict species without any close ally. However, our data point to a close relationship between these two endemics from the Canary Islands (Fig. 7).

Morphological characters used for classification: stamen types

Stamen morphology was used by Walker and Sytsma (2007) to distinguish two major lineages within Clade I. However, our analysis clearly shows that stamen morphology is much more variable. Character state reconstruction revealed that stamen type A (Supplementary Data Fig. S5) is the ancestral state for Clade III-A and Salvia s.s. (Clade I). Consequently, the reduction of the lower lever arm evolved several times in parallel. In Salvia s.s. (Fig. 8), sub-clade I-A covers the whole range of stamen modifications described in African Salvia (Fig. 8; Hedge, 1974), including the rare stamen type C (S. namaensis). In the OW, this stamen modification is only known from the Eurasian S. verticillata group (four species), which is also part of Salvia s.s. (Clade I; Will, 2013), but not closely related to S. namaensis from SSA. A third species with stamen type C and the same ontogeny as S. verticillata is Rosmarinus officinalis (unpubl. res.). Parallel evolution is thus evident (Supplementary Data Fig. S5), restricting the use of stamen types to lower taxonomic levels.

Fig. 8.

Fig. 8.

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Trends in the evolution of stamen types in African representatives of Salvia s.s. (Clade I). Proceeding from the ancestral stamen type A, the hypothetical stamen evolution is illustrated. Stamen of S. whitehousei modified after Whitehouse (1949), S. interrupta modified after Rosúa and Blanca (1986), schemata of all other stamens modified after Hedge (1974); filament (medium grey); connective (light grey); theca (dark grey); stamen types (in circles; ± A = reduced type A); and clades (I-A to I-D) represented by the species are given above the branches; scale bar = 5 mm.

Floristic links of Salvia spp. in North Africa

Salvia spp. distributed in North Africa are clearly members of two different clades (Fig. 7; I-A and III-A). Based on the molecular data, they show many floristic links to southern Europe, SW Asia, East and southern Africa (Fig. 5). One example is S. taraxacifolia, a relict species endemic to the High Atlas, Morocco (Hedge, 1974). It is most closely related to East (S. nilotica and S. somalensis) and southern African species (Fig. 7; I-A). Our data suggest dispersal from North to East Africa followed by a second dispersal to southern Africa. Salvia taraxacifolia and the two East African species are adapted to mesic habitats, whereas their southern African relatives prefer arid habitats (Fig. 9E–G). This indicates that the common ancestor of sub-clade I-A might have been adapted to mesic conditions and that within the large SSA radiation (sub-clade I-A), adaptation to arid localities evolved in southern Africa.

The floristic links between North Africa and southern Europe already proposed by Hedge (1974) (Fig. 7; sub-clade I-C) were confirmed by the close relationship of S. interrupta (SW Morocco; Fig. 10B: 56) and S. candelabrum (southern Spain; Fig. 10B). Both are thermophilic and partly overlap in their distribution (Fig. 10B; Rosúa and Blanca, 1986, 1990). They have a similar habit (divided leaves, most of them at the base of the stem), conspicuous, elongated inflorescences and the same chromosome number (2n = 14) (Hedge, 1974; Rosúa and Blanca, 1985, 1990). Salvia interrupta is considered as a Tertiary relict which was more widely distributed when the climate was more mesic (Rosúa and Blanca, 1990). Both species are obviously derived from a common, probably mesic-adapted, ancestor. Their relationship might reflect allopatric speciation probably triggered by different edaphic factors in the corresponding habitats.

The strongly supported sister relationship of S. daghestanica (Caucasus) and S. phlomoides subsp. phlomoides (North Africa and southern Europe; Fig. 10B: 47) reflects floristic links between the Mediterranean and SW Asia. Since contact between the African and Eurasia floras should have increased during the Messinian Salinity Crisis in the late Miocene [5·96–5·33 million years ago (Mya)], plant colonization across the Mediterranean is expected to have occurred often during this time frame (Caujapé-Castells and Jansen, 2003). We assume that this ‘route’ was also used repeatedly by Salvia. We thus support the hypothesis of Davis and Hedge (1971) that the SW Asian origin of some NW African species was triggered by a westward shift of Irano-Turanian elements.

Repeated colonization of the Canary Islands and long-distance dispersal in Salvia

The Macaronesian flora is composed of endemics derived from an ancient Tertiary relict flora and more recently introduced species (e.g. Helfgott et al., 2000; Manen et al., 2002; Carine et al., 2004). This general pattern also appears to hold for the Macaronesian S. canariensis, S. broussonetii and S. herbanica (Fig. 9B: 7–9). Since the three species clearly differ in their morphology (Fig. 4F–H) and habitat preference (Fig. 3D, G), they were never expected to be closely related (Hedge, 1974; Carine et al., 2004). However, S. canariensis and S. broussonetii are sister species forming one clade within sub-clade I-C (Figs 5 and 7). The proposed allies of S. canariensis (Hedge, 1974) are not closely related to these two species, thus contradicting Hedge's (1974) hypothesis of a link between the Canary Island and southern African Salvia.

In contrast, S. herbanica is found in a different clade (Fig. 7; III-A) and has clear links to species from East Africa and the Arabian Peninsula. Our findings indicate the non-monophyly of the Canary Island endemics and support the hypothesis of repeated dispersals to the archipelago from different mainland sources (Emerson et al., 2000; Arnedo et al., 2001; Fuertes-Aguilar et al., 2002; Carine et al., 2004, and references therein; Vargas, 2007).

The colonization of the Canary Islands raises the question of how dispersal might have taken place. The question of how (if at all) Salvia might be adapted to long-distance dispersal (LDD) is not yet answered. For the Canary Islands, the proximity to the African continent might have eased dispersal. The oldest islands, Lanzarote and Fuerteventura, are presently 100 km from the coast of North Africa (Francisco-Ortega et al., 2000; Acosta et al., 2005), but at some periods during the last 20 million years they were probably much closer (García-Talavera, 1997). García-Talavera (1997) suggested that the volcanic sea mounts served as ‘stepping stones’ when the sea level dropped during glacial periods. In addition, recent studies have assumed convective updraft to be the key mechanism for LDD of even heavy diaspores (Nathan et al., 2002; Tackenberg et al., 2003). Long-distance dispersal to the archipelago mediated by wind is conceivable for S. herbanica, S. aegyptiaca and their potential common ancestor. Salvia aegyptiaca is distributed within the area of the Saharan Air Layer, a westward-directed wind of comparably high velocity (Carlson and Prospero, 1972; Tackenberg et al., 2003)

East Africa and the Arabian Peninsula as ‘melting pots’ for Salvia

East African Salvia is found in three independent clades (Fig. 7; III-A, I-C and I-A) and consequently has various floristic links beyond the continent.

Salvia merjamie (sub-clade I-C; Fig. 9D: 16) is a frequent and extremely variable species in the montane forest belts from Ethiopia to Zimbabwe (Hedge, 1974). It is part of a strongly supported (ITS) clade with two widely distributed species from SW Asia. Salvia merjamie is moderately supported (ML) as the sister to S. verbenaca 141 from Turkey. Both are polymorphic, occasionally have cleistogamous flowers and share the chromosome number of 2n = 42, which is uncommon in Salvia (Reese, 1957; Gadella et al., 1966; Hedge, 1974; Hedberg and Hedberg, 1977; Haque and Ghoshal, 1980; Codd, 1985; Vogt and Aparicio, 1999; Foley et al., 2008).

Salvia nilotica (sub-clade I-A; Fig. 9D: 17) has a broader distribution range than S. merjamie. Hedge (1974) assumed that S. nilotica was a distinct, taxonomically isolated species but also discussed its similarities with species restricted to the eastern Cape. With S. taraxacifolia and S. somalensis, S. nilotica is found in a basal position of sub-clade I-A, suggesting a dispersal from North to southern Africa via East Africa. The relationship of S. nilotica and the African members of section Heterosphace Benth. proposed by Hedge (1974) is confirmed, since all of these species are placed in the same sub-clade (I-A).

Salvia deserti (sub-clade III-A; Fig. 9D: 14) is an endemic of the Egyptian and Arabian deserts (Boulos, 2008; Hedge, 1974; Migahid, 1978). It is morphologically and genetically distinct from Salvia s.s. Incongruences detected in nuclear and plastid data support a hybrid origin of this species.

Pollinator diversity and evolution of bird pollination in Sub-Saharan Africa

Based on flower morphology, bees are seen as the most important pollinators in Salvia overall (Wester and Claßen-Bockhoff, 2006, 2011). This was also assumed for the African and in particular for the southern African species (Hedge, 1974). However, only a limited number of field observations confirm this view, e.g. the first report of small bees on S. africana-caerulea (Marloth, 1908), data on Anthophora diversipes (Goldblatt et al., 2000a, b), and observations of Xylocopa caffra, Amegilla spp., further solitary bees and honey-bees by P. Wester, R. Claßen-Bockhoff and H. Technau (pers. comm.).

Flowers with long tubes and freely accessible pollen were expected to be pollinated by long-tongued insects, e.g. flies. This pollinator guild is characteristic for South Africa, especially in the western Cape Region (Goldblatt and Manning, 2000). Potgieter and Edwards (2001, 2005) assumed that S. scabra and S. repens are pollinated by long-tongued flies (Stenobasipteron wiedemanni and Prosoeca spp.), but field observations are still lacking.

Although bird pollination is quite frequent in NW Salvia (Wester and Claßen-Bockhoff, 2007), the only known ornithophilous Salvia spp. in the OW appear in southern Africa (Wester and Claßen-Bockhoff, 2006). Three, S. lanceolata, S. thermarum and S. africana-lutea, are restricted to southern Africa (Fig. 4I, R, S). Probably two more (S. leucodermis and S. sessilifolia; Fig. 4P, Q) occur in Madagascar. Our data confirm that ornithophily evolved repeatedly in the NW (Fig. 7), but also indicate at least two pollinator shifts from bee to bird pollination in Africa (Supplementary Data Fig. S6). Most probably, this pollination system evolved three times in parallel within sub-clade I-A: (1) in the Madagascan sub-clade; (2) in the S. africana-lutea and S. lanceolata clade; and (3) in S. thermarum. Including species adapted to bee, bird and, most probably, long-tongued fly pollination, sub-clade I-A represents a further example of a monophyletic lineage having undergone pollinator-driven diversification in southern African (e.g. Van der Niet and Johnson, 2012; Sun et al., 2014; Van der Niet et al., 2014).

In bird-pollinated species, bees are largely excluded from nectar access but not from collecting pollen. They might therefore trigger hybridization between bird- and bee-pollinated species (Van Jaarsveld, 2002; P. Wester, University of Düsseldorf, Germany, pers. comm.), e.g. in S. africana-caerulea. The species is morphologically well adapted to bee pollination but is also occasionally pollinated by birds (Wester, 2013). It might be a species in which the exploitation of a food plant by pollinators (birds) can be observed even though both species are not yet perfectly adapted to each other (Thomson and Wilson, 2008). Thus, S. africana-caerulea might represent an example of a pollinator shift in progress (Rodríguez-Gironés and Santamaría, 2004).

Conclusions

African Salvia is non-monophyletic. Continental Africa, the Canary Islands, East Africa and the Arabian Peninsula were each colonized repeatedly. The morphological diversity of African sage results from independent dispersals from different mainland sources and diversification in the diverse African environment. Parallel evolution played an important role for the evolution of stamen types, calyx enlargement and pollination syndrome. These data can even be transferred to Salvia s.l. for which similar trends have been observed.

SUPPLEMENTARY DATA

Supplementary data are available online at www.aob.oxfordjournals.org and consist of the following. Table S1: character states coded for the ancestral character state reconstruction with references. Figure S1: analyses of the ETS data set (ML and BI). Figure S2: reconstruction of the ancestral distribution of Sub-Saharan African Salvia. Figure S3: ancestral character state reconstruction of the life form in Sub-Saharan African Salvia. Figure S4: ancestral character state reconstruction of the calyx morphology in Sub-Saharan African Salvia. Figure S5: ancestral character state reconstruction of the stamen morphology in Sub-Saharan African Salvia. Figure S6: ancestral character state reconstruction of the pollination syndrome in Sub-Saharan African Salvia.

Supplementary Data
supp_114_1_61__index.html (714B, html)

ACKNOWLEDGEMENTS

We thank Dirk Albach (Oldenburg), Safi Bagherpour (Ankara), Benny Bytebier (KwaZulu-Natal), Ferhat Celep (Nevşehir), Ahmet El-Banhawy (Ismailia/Redding), Ahmed Kahraman (Ankara), Alexander P. Sukhorukov (Moscow), Mats Thulin (Uppsala) and Petra Wester (Düsseldorf) for sampling, and the following herbaria for offering plant material: ACECR (Iran), B, E, EA, GOET, HUH, M, MJG, MO, MPU and MW. Photographs were kindly provided by Ferhat Celep, Rafael N. B. Groneberg (Mainz), Dylan Hannon (San Marino, CA), Peter B. Phillipson (Paris), Hen Technau, Mats Thulin and Petra Wester. We thank Berit Gehrke and Michael D. Pirie (both Mainz) for assistance with data analyses, and Natalie Schmalz, Abigail J. Moore (Providence, RI) and two anonymous reviewers for helpful comments to improve the manuscript. This work was supported by the DFG (Deutsche Forschungsgemeinschaft; Cl 81/10–1) and the Fachbereich Biologie (Universität Mainz).

APPENDIX: PLANT MATERIAL INCLUDED IN THIS STUDY

For all sequences generated by the first author, a DNA accession number is given

Taxon Locality Voucher collector with collection no. (herbarium) DNA acc. no. GenBank accession no.
    rpl32-trnL nrITS ETS
Clinopodium dalmaticum (Benth.) Bräuchler & Heubl M. Kintgen s.n. – JQ669340 – –
Clinopodium taxifolium (Kunth) Govaerts B. Drew 228 – JQ669288 – –
Clinopodium vulgare L. Riina 1579 – JQ669290 – –
Collinsonia canadensis L. JBW 958 – – DQ667248 –
Raiche s.n. UCBG 1984.0696 – JQ669291 – JQ669157
Dorystaechas hastata Boiss. & Heldr. ex Benth. Anatolia Albach D6–4 (OLD) 213 KJ747319 KJ584248 KJ584275
Cult. RBGE1972–0177D – JQ669302 DQ667252 –
– – HQ418845 –
Glechoma hederacea L. B. Drew 69 – JQ669307 – –
Horminum pyrenaicum L. Cult. RBGE 1997–2109a – JQ669315 DQ667257 –
M. Will 63 (MJG 003069) 390 KJ747327 KJ584247 KJ584279
Hyptis laniflora Benth. B. Drew 41 – JQ669317 – –
Isolate K36721 – – JF301548 JF404259
Lepechinia bella Epling Bolivia P. Wester 145 (MJG 009474) 216 KJ747326 – –
Lepechinia calycina (Benth.) Epling ex Munz Drew 197 – JQ669324 – –
Lepechinia conferta Epling Alonso 8376 (F) – – DQ667307 –
Lepechinia lamiifolia (Benth.) Epling B. Drew 178 – JQ669325 – –
Lepechinia lancifolia (Rusby) Epling Smith 444 (F) – – DQ667306 –
Lepechinia mexicana (S.Schauer) Epling B. Drew 164 – JQ669326 – –
Melissa axillaris (Benth.) Bakh.f. D. E. Boufford et al. 24526 – JQ669334 – –
Melissa officinalis L. M. Will 64 (MJG 003068) 388 KJ747325 KJ584249 KJ584285
JBW 2575 (cult. USA/WIS) – – DQ667291 –
B. Drew 70 – JQ669335 JF301353 –
Mentha arvensis L. B. Drew 82 – JQ669336 – –
Mentha pulegium L. Riina 1574 – JQ669338 – –
Mentha spicata L. J. Walker 2566 – JQ669339 – –
Mentha spicata subsp. condensata (Briq.) Greuter & Burdet Riina 1575 – JQ669337 – –
Meriandra bengalensis (Konig ex Roxb.) Benth. Lavranus & Newton 15796 (MO 2633828) – – DQ667329 –
Perilla frutescens (L.) Britton JBW 1078 (cult. USA/WIS) – – DQ667246 JF301326
Perovskia atriplicifolia Benth. M. Will 65 (MJG 003070) 472 – KJ584242 –
  JBW 2524 (cult. USA/WIS) – JQ669352 DQ667223 JF301328
Perovskia scrophulariifolia Bunge Kinziraeva 6751 (MO 5201778) – – DQ667330 –
Rosmarinus officinalis L. M. Will 66 (MJG 003071) 389 KJ747310 KJ584197 KJ584296
  JBW 2558 (cult. USA/WIS) – JQ669364 DQ667241 –
Salvia aegyptiaca L. M. Kuschewitz s.n. (cult. BG HH) 204 KJ747314 KJ584245 KJ584254
  McLeish 3728 (E) – – DQ667285 –
S. aethiopis L. Armenia J. Hellwig s.n. 26/6/02 (MJG 009919) 281 – KJ584163 –
  Armenia J. Hellwig s.n. 26/6/02 (MJG 009919) – – DQ667272 –
S. africana-caerulea L. S Africa P. Wester & R. Claßen-Bockhoff 319 (MJG 041401) 230 KJ747271 KJ584204 KJ584255
  S Africa P. Wester & R. Claßen-Bockhoff 317 (MJG 041402) 229 – KJ584203 –
S. africana-lutea L. S Africa P. Wester 342 (MJG 041393) 81 KJ747273 KJ584205 KJ584256
  S Africa P. Wester 708 (MJG) 234 KJ747259 – –
  S Africa P. Wester 708 (MJG) 430 KJ747272 – –
S. albicaulis Benth. S Africa P. Wester, R. Claßen-Bockhoff & E. v. Jaarsveld 340 (MJG 041403) 1 KJ747274 KJ584206 KJ584257
S. albicaulis × granitica S Africa P. Wester, R. Claßen-Bockhoff & E. v. Jaarsveld 341 (MJG 041404) 2 KJ747275 KJ584207 KJ584258
  S Africa P. Wester, R. Claßen-Bockhoff & E. v. Jaarsveld 341 (MJG 041404) 42 – KJ584215 KJ584277
S. apiana Jeps. California P. Wester 411 (MJG 041452) 392 KJ747321 – –
  JBW 2509 USA (WIS) – – DQ667214 –
S. areysiana Deflers Yemen Thulin, Eriksson, Gifri & Långström 8472 (UPS) 282 KJ747315 – KJ584259
S. argentea L. Italy R. Claßen-Bockhoff s.n. Mai 2002 (MJG) 57 KJ747299 KJ584164 –
S. aristata Aucher Iran K.H. Rechinger s.n. 1974 (M) 289 – KJ584244 –
  Iran Y. Ajani 1569 (ACECR) 417 KJ747264 – –
  Wedelbo & Assadi s.n. (E) – JQ669365 DQ667280 JF301336
S. aucheri var. canescens Boiss. & Heldr. Anatolia F. Celep 1245 (PSL METU) 239 – KJ584193 –
  Archibald 7670 (E) – – DQ667286 –
S. aurita L.f. P. Wester & R. Claßen-Bockhoff 324 (MJG 041405) 11/424 KJ747276 KJ584218 KJ584261
  M. Will 26 (MJG 041563) 423 – KJ584219 KJ584260
S. aurita var. galpinii (Skan) Hedge P. Wester 472 (MJG) 425 KJ747269 – –
S. austriaca Jacq. R. Claßen-Bockhoff s.n. 2004 (cult. BG Mz) – – DQ667323 –
  Austria R. Claßen-Bockhoff s.n. 12.06.2003 (MJG) 280 KJ747261 – –
S. bariensis Thulin Somalia M. Thulin, A. Dahir & A. Osman 9429 (UPS) 283 KJ747316 – KJ584262
S. broussonetii Benth. M. Will 33 (MJG 041537) 29 KJ747293 KJ584226 KJ584263
  Tenerife R. Claßen-Bockhoff 2/10 (MJG 009887) 463 – KJ584225 KJ584264
S. cabulica Benth. Afghanistan H. Freitag 4683 (MSB 137713) 322 – KJ584189 –
  Ghafoor & Goodman 5148 (E) – – DQ667287 –
S. canariensis L. M. Will 46 (MJG 041565) 5 KJ747295 KJ584227 KJ584266
  Tenerife R. Claßen-Bockhoff 3/10 (MJG) 464 – – KJ584265
  Tenerife R. Claßen-Bockhoff 1/03 (MJG) 223 KJ747294 – –
  Cult. RBGE 1986–0478 – – DQ667256 –
S. candelabrum Boiss. M. Will 42 (MJG 041557) 62 KJ747255 KJ584190 –
S. candidissima subsp. occidentalis Hedge Anatolia F. Celep 1487 (PSL METU) 201 KJ747300 KJ584165 –
S. candidissima Vahl. Cult. RBGE 1999–2202A – – DQ667261 –
S. chamelaeagnea Berg. P. Wester & R. Claßen-Bockhoff 314 (MJG 041407) 52 KJ747289 KJ584210 KJ584268
  S Africa P. Wester, R. Claßen-Bockhoff & E. Van Jaarsveld 313 (MJG 041406) 432 – KJ584211 KJ584267
  M. Will 47 (MJG 041541) 433 – KJ584212 –
S. chienii E. Peter M. Will 61 (MJG 003066) 53 KJ747322 KJ584250 –
  AnH0305–21 – – DQ132868 –
S. chionopeplica Epling JBW 2545 (cult. USA/WIS) – – DQ667227 –
S. cf. chionopeplica Epling P. Wester 485 (MJG 041435) 174 KJ747318 KJ584188 KJ584269
S. daghestanica Sosn. M. Will 34 (MJG 041551) 276 KJ747308 KJ584187 –
  Cult. RGB E 1988–2283A – – DQ667258 –
S. deserta Schang M. Will 96 (MJG 003100) 286 KJ747263 KJ584176 –
  XingJ0305–1 – – DQ132865 –
S. deserti Dcne. Egypt E. Gamal Eldin s.n. 3.5.1991 (GOET) 335 KJ747312 – KJ584270
S. disermas L. P. Wester & R. Claßen-Bockhoff 326 (MJG 041413) 15 KJ747296 KJ584179 KJ584271
  M. Will 80 (MJG 003116) 454 – – KJ584272
S. disermas L. (syn. S. rugosa in GenBank) Goldblatt 7500 (E) – – DQ667290 –
S. dolomitica Codd P. Wester & R. Claßen-Bockhoff 321 (MJG 041411) 82 KJ747290 KJ584214 KJ584274
  F. Brusse 5610 (M) 440 – KJ584213 KJ584273
  JBW 3200 (cult. USA/WIS) – – DQ667322 –
S. dominica L. Cyprus A. Seregin, D. Sokoloff & M. Remizova A-211 (MW) 267 – KJ584167 –
  M. Kuschewitz s.n. (MJG 009323) 217 KJ747262 KJ584166 –
S. evansiana Hand.-Mazz. var. evansiana M. Will 55 (MJG 003060) 415 KJ747323 KJ584251 –
S. freyniana Bornm. Anatolia S. Bagherpour 493 (PSL METU) 98 KJ747266 – –
S. fruticosa Miller Anatolia F. Celep 1373 (PSL METU) 100 KJ747256 KJ584195 –
  G. Hausner GR 31 (MJG 003078) 66 – KJ584194 –
S. funerea Jones P. Wester 490 (MJG 041430) 393 KJ747320 – –
S. garipensis E.Meyer ex Benth. Strohbach 149 (E) – – DQ667281 –
S. geminata Thulin Yemen M. Thulin, Beier & M. Hussein 9629 (UPS) 341 – – KJ584276
S. glutinosa L. Anatolia F. Celep 1196 (PSL METU) 101 – KJ584253 –
  JBW 2568 (cult. USA/WIS) – – DQ667250 –
S. graciliramulosa Epling & Játiva Bolivia P. Wester 14 (MJG 041090) – – DQ667276 –
S. gretai Brandegee USA JBW 2511 (WIS) – JQ669367 DQ667215 JF301331
S. henryi Gray USA JBW 2516 (WIS) – – DQ667216 –
S. herbanica A.Santos & M.Fernández Fuerteventura R. Claßen-Bockhoff 1/05 (MJG 009888) 40 KJ747313 KJ584246 KJ584278
S. heterochroa Fern. Yunnan, China D. E. Boufford, J. H. Chen, S. L. Kelley, R. H. Ree, H. Sun, B. Xü, J. P. Yue, L. L. Yue, D. C. Zhang & W. D. Zhu 35205 (HUH 286716) 252 KJ747324 KJ584252 –
S. hydrangea Benth. Anatolia A. Kahraman 1468 (PSL METU) 242 KJ747257 KJ584192 –
  Rechinger 47123 (E) – – DQ667288 –
S. hydrangea Benth. (syn. S. dracocepha-loides Boiss. in GenBank) Armenia Hellwig s.n. (MJG 009920) – – DQ667265 –
S. interrupta Schousb. M. Will 30 (MJG 041550) 447 KJ747265 KJ584191 –
S. judaica Boiss. M. Will 57 (MJG 003061) 409 – KJ584241 –
S. lanceolata Lam. P. Wester 316 (MJG 041396) 58 KJ747278 KJ584202 KJ584281
  S Africa P. Wester 1129 (NBG) 264 KJ747277 KJ584201 KJ584280
S. lanceolata × africana-caerulea P. Wester & R. Claßen-Bockhoff 315 (MJG 041400) 236 KJ747279 KJ584216 KJ584282
S. lanigera Poir. Sinai A. El-Banhawy 11 (University of Ismailia, Egypt) 198 – KJ584185 –
S. leucodermis Baker Madagascar R. A. Clement, P. B. Phillipson & G. Rafamantanantsoa 2137 (E 00161484) 348 KJ747280 KJ584220 KJ584284
  Madagascar P. Wester 1131 (TAN) 459 – KJ584221 –
  Madagascar B. Bytebier 3193 (TAN) 460 – KJ584222 KJ584283
S. merjamie Forsk. M. Will 83 (MJG 003113) 265 KJ747297 KJ584184 KJ584286
S. microstegia Boiss. & Bal. Armenia J. Hellwig s.n. (MJG 009884) 212 KJ747307 KJ584171 –
S. microstegia Boiss. & Bal. (S. verbascifolia M.Bieb.in GenBank) Armenia J. Hellwig s.n. (MJG 009884) – – DQ667264 –
S. muirii L.Bolus P. Wester & R. Claßen-Bockhoff 328 (MJG 041409) 162 KJ747283 KJ584208 KJ584287
  P. Wester & R. Claßen-Bockhoff 318 (MJG 041410) 163 – KJ584209 KJ584288
S. namaensis Schinz M. Will 28 (MJG 041552) 435 KJ747284 KJ584217 KJ584290
  P. Wester & R. Claßen-Bockhoff 330 (MJG 041415) 78 KJ747281 KJ584234 KJ584291
  SW Africa W. Giess & M. Müller 14319 (M) 296 – KJ584200 KJ584289
S. nilotica Juss. ex Jacq. U. Hecker g3186 (MJG 003079) 64 – KJ584230 –
  M. Will 49 (MJG 041538) 436 KJ747258 KJ584229 KJ584292
S. officinalis L. JBW 2580 (cult. USA/WIS) – – DQ667225 –
  Voucher 2160 – JQ771324 – –
  M. Palma s.n. UCBG 7·0083 – JQ669369 JF301355 JF301332
  N Africa A. El-Banhawy 16 (University of Ismailia, Egypt) 243 – KJ584196 –
S. palaestina Benth. Anatolia F. Celep 1083 (PSL METU) 400 KJ747304 KJ584175 –
  Anatolia A. Kahraman 1443 (PSL METU) 125 KJ747301 – –
S. cf. palaestina Benth. N Africa A. El-Banhawy 6 (University of Ismailia, Egypt) 200 KJ747302 KJ584172 –
S. patens Cav. Cult RBGE 1973–9197 – JQ669370 DQ667253 JF301333
S. penstemonoides Kunth & Bouché JBW 2578 (cult. USA/WIS) – – DQ667221 –
S. phlomoides ssp. phlomoides Asso Morocco R. Vogt 10336 & Ch. Oberprieler 4784 (B 100145114) 337 KJ747309 KJ584186 –
S. polystachya Ort. Breedlove & Mahoney 72286 (UC) cult. UCBG 92·052 – JQ669371 – JF301334
S. pratensis L. C Russia A. Suchorukow s.n. VII 2003 (MW) 275 KJ747291 KJ584178 –
  Isolate S0628 – – EU169486 –
S. przewalskii Maxim. Cult. RBGE 1993–2067A – JQ669372 DQ667254 JF301339
S. radula Benth. S Africa Germishuizen 3950 (MO 4385830) 328 – KJ584180 KJ584293
S. repens Burch. ex Benth. M. Will 50 (MJG 041931) 61 KJ747282 KJ584232 KJ584295
S. cf. repens Burch. ex Benth. P. Wester & R. Claßen-Bockhoff 325 (MJG 041412) 437 – KJ584231 KJ584294
S. roemeriana Scheele USA JBW 2515 (WIS) – – DQ667211 –
S. scabra L. M. Will 37 (MJG 041549) 55 KJ747285 KJ584233 KJ584297
S. schimperi Benth. Yemen D. Podlech 36057 (M 55003) 310 – KJ584174 KJ584298
  M. Will 72 (MJG 003099) 466 – KJ584168 –
S. schlechteri Briq. P. Wester & R. Claßen-Bockhoff 323a (MJG 041416) 31 KJ747286 KJ584235 KJ584299
  M. Will 51 (MJG 041539) 438 – KJ584236 KJ584300
S. sclarea L. Anatolia F. Celep 1492 (PSL METU) 244 KJ747305 KJ584162 KJ584301
  JBW 2527 (cult. USA/WIS) – JQ669373 DQ667222 –
S. sessilifolia Baker Madagascar R. A. Clement, P. B. Phillipson & G. Rafamantanantsoa 2001 (MO 4328854) 331 – KJ584223 KJ584302
  Madagascar C. H. Jongkind & S. Rapanarivo 929 (MO 4870099) 332 – KJ584224 KJ584303
  Madagascar Jongkind & Rapanarivo 929 (E) – – DQ667282 –
S. somalensis Vatke M. Will 77 (MJG 003119) 340 KJ747311 KJ584240 KJ584304
S. spinosa L. N Africa A. El-Banhawy 14 (University of Ismailia, Egypt) 199 KJ747303 KJ584173 –
S. stenophylla Burch. ex Benth. S Africa Burgoyne & Snow 4805 (MO 5649981) 330 KJ747260 KJ584237 KJ584305
  Giess & Hübsch 11607 (M) 439 – KJ584238 KJ584306
S. summa A. Nelson Texas JBW 1972 USA (WIS) – – DQ667217 –
  Texas P. Wester 373 (MJG 041338) 190 – – KJ584307
S. sylvestris L. Anatolia A. Kahraman 1568 (PSL METU) 118 KJ747292 KJ584181 –
(syn. S. tesquicola Kiok. & Pobed.) C Russia A. Suchorukow s.n. VIII 1994 (MW) 273 – KJ584177 –
  Isolate S0626 – – EU169485 –
S. taraxacifolia Hook.f. Morocco W. Lippert 25355 (M) 304 KJ747270 KJ584228 KJ584308
  JBW 2521 (cult. USA/WIS) – – DQ667209 –
S. texana (Scheele) Torr. Texas P. Wester 362 (MJG 041477) 191 KJ747267 KJ584199 –
  Texas P. Wester 362 (MJG 041477) – – DQ667321 –
S. thermarum Van Jaarsv. P. Wester & R. Claßen-Bockhoff 336 (MJG 041398) 23 KJ747288 KJ584239 KJ584309
  M. Will 52 (MJG 041933) 452 – – KJ584310
  S Africa P. Wester 312 (MJG 041397) 221 KJ747287 – –
S. tingitana Etling Morocco D. Podlech 43384 (M 54979) 314 – KJ584169 –
S. trichocalycina Benth. Breckle 4963 (E) – – DQ667283 –
S. trijuga Diels YunN0309–5 – – DQ132870 –
S. veneris Hedge Cyprus M. J. Y. Foley 1701 (E 00147797) 413 KJ747306 KJ584170 –
S. verbenaca L. Syria W. Licht SYR 307 (MJG 003082) 67 – KJ584182 –
  Anatolia F. Celep 1408 (PSL METU) 141 KJ747298 KJ584183 –
S. whitehousei Alziar Texas P. Wester 352 (MJG 041389) 231 KJ747268 KJ584198 KJ584311
  Texas P. Wester 352 (MJG 041389) – – DQ667320 –
Thymus pulegioides L. Riina 1577 – JQ669378 – –
Thymus serpyllum L. J. Walker 2564 (cult. USA/WIS) – JQ669379 – –
Zhumeria majdae Rech.f. & Wendelbo Iran F. Sharififar 1651 (ACECR) 422 KJ747317 KJ584243 KJ584312
  Wendelbo 15793 (V 21730) – – DQ667336 –
  Ghazi s.n. (V 01176) – – DQ667335 –
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acc. no., accession number; locality: origin from natural habitats confirmed; ACECR, Iranian Academic Center for Education Culture and Research; 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.

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