An updated subtribal classification of the Compositae–Anthemideae is presented based on gene- and species-tree reconstructions considering sequence variation from the plastid (cpDNA ndhF, trnL-trnF) and nuclear genome (nrDNA ITS1-5.8S-ITS2, ETS; nDNA dual specificity phosphatase DSP, plus-3 domain-containing protein of the vernalization independence 5 complex VIP5, major facilitator superfamily protein of the Nitrate Transporter1/Peptide Transporter NPF3.1) for 113 of the 115 hitherto accepted genera of the tribe. As a result, six subtribes are newly circumscribed, i.e. Anthemidinae (including also Xylanthemum), Artemisiinae (including also Hulteniella, Lepidolopha, Opisthopappus and Tridactylina), Glebionidinae (including also Otoglyphis, Endopappus and Nivellea), Handeliinae (including Cancrinia, Polychrysum and excluding Xylanthemum), Leucantheminae (including also Daveaua, Heteromera and Otospermum) and Leucanthemopsidinae (including Phalacrocarpum). Additionally, five unigeneric subtribes (i.e. Brocchiinae, Inulantherinae, Lepidophorinae, Lonadinae and Vogtiinae) are described as new to science due to their phylogenetically isolated positions, resulting in 19 subtribes accepted for Compositae–Anthemideae. Three new combinations are proposed to accommodate the former Aaronsohnia factorovskyi Warb. & Eig and A. pubescens subsp. maroccana (Ball) Fennane & Ibn Tattou in the genus Otoglyphis Pomel (1874), which was found to have priority over Aaronsohnia Warb. & Eig (1927), and to accommodate the former Tanacetum paleaceum Podlech in the genus Xylanthemum Tzvelev.
Citation: Oberprieler C., Töpfer A., Dorfner M., Stock M. & Vogt R. 2022: An updated subtribal classification of Compositae tribe Anthemideae based on extended phylogenetic reconstructions. – Willdenowia 52: 117–149.
Version of record first published online on 18 May 2022 ahead of inclusion in April 2022 issue.
Introduction
The chamomile tribe of the sunflower family (Compositae–Anthemideae) comprises more than 100 genera and around 1800 species (Oberprieler & al. 2006, 2009). A subtribal classification of the tribe was proposed by Bremer & Humphries (1993) in a generic monograph of the Anthemideae and was mainly based on morphological characters. However, in subsequent molecular phylogenetic studies, many of the subtribes erected by Bremer & Humphries (1993) turned out to be non-monophyletic, and a new subtribal classification was proposed by Oberprieler & al. (2007, 2009) based on nrDNA ITS and cpDNA ndhF sequence variation. Due to the lack of plant material for a number of genera or their unresolved positions in the mentioned phylogenetic analyses, the subtribal classification of Oberprieler & al. (2007, 2009) still comprised a number of orphan genera, for which a subtribal assignment was not possible. For some of these, the present contribution tries to determine their subtribal placement and their generic relationships based on adding sequence information from an additional nuclear multi-copy (nrDNA ETS), three low-copy nuclear markers and from the faster evolving cpDNA intergenic spacer region trnL-trnF.
Material and methods
Plant material and DNA sequencing — The selection of taxa and specimens studied in the present contribution was based on the previous circumscription of genera of the Anthemideae (Oberprieler & al. 2007, 2009), with the addition of representatives of the hitherto subtribally unclassified genera (Appendix 1). Total genomic DNA was extracted following the modified protocol of the CTAB method (Doyle and Doyle 1987; Doyle and Dickson 1987).
PCR amplicons of nrDNA ITS were gained using the following primers: ITS2, ITS4, ITS5 (White & al. 1990), ITS5 (Downie & Katz-Downie 1996), ITS-18SF, ITS-26SR (Rydin & al. 2004), P1 (Ochsmann 2000), ITS-D (Blattner 1999) and ITS-SR (Blattner & al. 2002). For the amplification of nrDNA ETS, we used the primers LETS (Lee & al. 2002) and 18S-ETS (Baldwin & Markos 1998). The plastid gene ndhF was amplified with the primers ndhF-1260, ndhF-3′Forward and ndhF-3′Reverse (Eldenäs & al. 1999) and the intergenic spacer region trnL-trnF with the primers trnL(e) and trnF(f) (Taberlet & al. 1991). The three novel single- or low-copy nuclear markers used in the present contribution were designed with the help of Leucanthemum Mill. consensus sequences (from the four species L. vulgare Lam., L. gaudinii Dalla Torre, L. monspeliense (L.) H. J. Coste and L. rotundifolium DC.) generated from clusters of Nanopore sequence reads, which were obtained during a previous target enrichment experiment (Scheunert & al. unpublished). For this purpose, particularly exon-rich consensus sequences were blasted against the genomes of Helianthus annuus L. (NCBI gene bank assembly accession: GCA_002127325) and Artemisia annua L. (NCBI gene bank assembly accession: GCA_003112345) and resulting alignments were used for primer design. Sequence sections that appeared to be suitable were analysed with Primer3Plus (Untergasser & al. 2012), and the primer sequences were checked for suitability with OligoCalc (Kibbe 2007) and Multiple Primer Analyzer (Thermo Fisher Scientific Inc., Waltham, MA, U.S.A.). Primer information and NCBI (National Center for Biotechnology Information) GenBank information on primer positions on the Artemisia annua L. genome are given in Table 1. The different marker names are based on the Arabidopsis thaliana (L.) Heynh. genome (At), where they were annotated as At1g18593 coding for the dual specificity phosphatase (DSP), At1g61040 coding for the plus-3 domain-containing protein, which is part of the vernalization independence 5 (VIP5) complex, and At1g68570 coding for the major facilitator superfamily protein, which is part of the Nitrate Transporter1/Peptide Transporter (NPF3.1).
Table 1.
Description of and primer information for the three nuclear single- or low-copy markers used in the present study. All three markers were gained by comparing genomic information for Helianthus annuus L. and Artemisia annua L. with reads from a target-enrichment experiment in Leucanthemum Mill. Selected loci are characterized by their positions on the Artemisia annua genome.
After purification of PCR amplicons with AMPure (Agencourt Bioscience Corp., Beverly, MA, U.S.A.) or AmpliClean (Nimagen, Nijmegen, The Netherlands) magnetic beads, Sanger sequencing was carried out by a contract sequencing company (Macrogen Europe, Amsterdam, The Netherlands). Electropherograms were edited with Chromas v2.6.6 (Technelysium Pty Ltd 1998–2018) with usage of the IUPAC code for polymorphisms, and marker-wise alignments were done with BioEdit v7.2.5 (Hall 1999) and the Mafft algorithm (Katoh & Standley 2013; Katoh & al. 2019).
Phylogenetic analyses — As outgroups for the analyses of both nrDNA ITS and cpDNA ndhF and trnL-trnF, we used nine species of the tribes Astereae, Calenduleae and Gnaphalieae (Appendix 1). In the phylogenetic reconstructions based on the combined datasets (both in the concatenated and in the coalescent-based species-tree reconstructions), the lack of complete sequence information for any of these outgroup taxa impeded rooting of the resulting species trees. Since the present phylogenetic reconstructions mainly aimed at the analysis and circumscription of subtribes in terms of monophyletic groups, we considered the placement of a tree root of secondary importance and rooted the species trees on the longest internal branch (i.e. the branch leading to Inulanthera and Ursinia).
For gene-tree reconstructions in MrBayes v3.2.7 (Huelsenbeck & Ronquist 2001; Ronquist & Huelsenbeck 2003; Ronquist & al. 2012), the General Time-reversible (GTR+I+G) model was found to be the best-fit sequence evolution model by using the “Automated Model Selection” option in PAUP* v.4.0a169 (Swofford 2021). Each gene-tree reconstruction was performed both with and without a coding of indels (done with GapCoder v.4; Young & Healy 2003) and the splitting of data into a DNA and a “coded gaps” partition. The latter partition was modelled with an equal-rates parameter. The gene-tree analyses for individual markers and the species-tree analysis based on the concatenated dataset were run in MrbAyes for 4 million to 150 million generations in two parallel runs with four chains each and a temperature of 0.02–0.1 on a workstation with ten cores until convergence of runs was attained (average standard deviation of split frequencies < 0.01).
Species-tree reconstruction based on a multispecies-coalescent model was performed with Beast v2.6.6 (Bouckaert & al. 2014, 2019) after creating the input file comprising the three nDNA markers of DSP, VIP5 and NPF3.1, the two cpDNA markers ndhF and trnL-trnF and the concatenated nrDNA ITS/ETS alignment with BEAUti (Drummond & al. 2012) using the StarBeast template. Substitution models assigned to the individual markers were the same as those used for the gene-tree analyses (GTR+I+G). For all partitions, the “Relaxed clock Log Normal” clock type, a Yule tree prior and a random starting tree were chosen. Priors were left at the default values, except for the uncorrelated lognormal relaxed clock means (“ucldMean”), which were modelled as a gamma distribution with the Alpha value at 0.2 and the Beta at 5.0. The chain length was set to 150 million and every 5000th generation was recorded. Runs were repeated until all operators were adjusted according to the suggestions given after each run was finished. The finalized BEAUti setup was run nine times using Beast v2.6.6. The convergence of independent runs was checked using Tracer v1.7.2. (Rambaut & al. 2018). Five of the resulting log and tree files that had converged best based on their “Effective Sample Size” values were combined using LogCombiner v2.6.6 with a burn-in of 20% and 30% until all ESS values of the finalized files were >200. TreeAnnotator v2.6.6 was then used to combine the 117,005 post-burn-in trees into a maximum-clade-credibility tree. TreeGraph v2.15.0-887beta (Stöver & Müller 2010) was used to edit the tree files.
Results and Discussion
Gene-tree reconstructions — The alignment of the traditionally Sanger sequenced plastid gene ndhF and the intergenic spacer region trnL-trnF is 1685 bp long ( Online Resource S1 (wi.52.52108_OnlineResource_S1.nex); including gap-coding information) and resulted in a phylogenetic tree with some well-supported monophyletic groups (Fig. 1). When compared with the phylogenetic tree based on ndhF information alone and comprising far fewer representatives of the tribe (Oberprieler & al. 2009), many topological features observed in this former phylogenetic reconstruction with its 62 taxa receive corroboration by being congruent to the present reconstruction based on 107 Anthemideae generic representatives: (1) the monophyly of subtribe Cotulinae; (2) the isolated position of Osmitopsis; (3) the sister-group relationship of Ursinia (Ursiniinae) and Inulanthera (hitherto unassigned to a subtribe); (4) the paraphyly of subtribe Athanasiinae; (5) the monophyly of all remaining subtribes comprising both subtribes centred in the S hemisphere (Pentziinae, Phymasperminae) and N hemisphere; (6) the lack of resolution among the subtribes of the “Asian-southern African grade” (Oberprieler & al. 2009; i.e. Artemisiinae, Handeliinae, Pentziinae and Phymasperminae); (7) the monophyly of the subtribes of the “Eurasian grade” and the “Mediterranean clade” (Oberprieler & al. 2009); (8) the lack of a clear demarcation between Anthemidinae and Matricariinae in the former; and (9) the clear monophyly of the latter (i.e. Glebionidinae, Leucantheminae and Santolininae). Additionally, many orphan genera missing from the previous analysis and hitherto unassigned to a subtribe now show well-supported subtribal affiliations that were only speculated upon by Oberprieler & al. (2009): (1) Cancrinia, Polychrysum and Ugamia in Handeliinae; (2) Phalacrocarpum in Leucanthemopsidinae; (3) Daveaua, Heteromera and Otospermum in Leucantheminae; and (4) Endopappus, Nivellea and Otoglyphis (the former Aaronsohnia, see below) in Glebionidinae. In contrast to this, other genera unassigned to a subtribe in our previous study are also found to be phylogenetically isolated here (i.e. Brocchia, Lepidophorum, Lonas and Vogtia).
The length of the alignment of the nuclear ribosomal repeat (nrDNA ITS) is 710 bp long ( Online Resource S2 (wi.52.52108_OnlineResource_S2.nex)), comprising ITS1 (alignment positions 1–293), the 5.8S gene (294–462) and ITS2 (463–710). The resulting phylogenetic reconstruction (Fig. 2) was found to be largely in accordance with the one based on plastid DNA sequence variation. It corroborates: the early divergence of Cotulinae and Osmitopsidinae; the paraphyly of Athanasiinae (with Phymasperminae nested within this anyway non-monophyletic generic assemblage); the inclusion of the S hemisphere subtribe Pentziinae into the large monophyletic group of all N hemisphere-centred subtribes); the close relationship among the circum-Mediterranean subtribes (Anthemidinae, Glebionidinae, Leucantheminae, Leucanthemopsidinae, Matricariinae and Santolininae); and the monophyly of the vast majority of previously described subtribes (except the already mentioned Athansiinae). Additionally, most of the above-mentioned subtribal affiliations of hitherto unclassified genera seen in the phylogenetic tree based on the two plastid markers receive further support from the nrDNA ITS tree; the exceptions being Endopappus and Phalacrocarpum, which lack supported placement in Glebionidinae and Leucanthemopsidinae, respectively.
The alignments of the three single-copy nuclear markers DSP, VIP5 and NPF3.1 are 264 bp (and additional 12 coded indels), 205 bp (without indels coding) and 458 bp long (without indels coding), respectively ( Online Resources S3 (wi.52.52108_OnlineResource_S3.nex)– S5 (wi.52.52108_OnlineResource_S5.nex)). Phylogenetic trees based on these three markers individually received much less-supported topologies ( Online Fig. S1 (wi.52.52108_OnlineFig_S1.pdf)– S3 (wi.52.52108_OnlineFig_S3.pdf)) but contained some strongly supported backbone and terminal branches. We hoped these would contribute additional support to the subtribal classification of orphan genera and the phylogenetic relationships among subtribes in the total-evidence approaches of the downstream species-tree reconstructions (see below). Owing to the patchy sampling of sequence information from the multi-copy nrDNA ETS marker (see Appendix 1), we decided to include it only in the species-tree reconstructions, in which only accessions with the majority of markers sampled were taken into account.
Species-tree reconstructions — The concatenated alignment of the total dataset is 3860 bp long ( Online Resource S6 (wi.52.52108_OnlineResource_S6.nex)), comprising markers DSP (alignment positions 1–241), VIP5 (positions 242–446), NPF3.1 (positions 447–904), ITS+ETS (positions 905–2389), ndhF (positions 2390–3401) and trnL-trnF (positions 3402–3860), and resulted in the phylogenetic tree shown in Fig. 3. The corresponding species tree received from the coalescent-based analysis of the same data set is depicted in Fig. 4. Owing to the lack of sequence information for all members of the outgroup and a considerable number of ingroup taxa, the two species-tree reconstructions differ from the gene trees mostly concerning the position of the root of the trees and the relationship among the early-diverging lineages of the tribe. However, when posterior probabilities along the backbone of the tree are considered, it becomes clear that there is only support from the analysis based on concatenated sequences (Fig. 3) that the earliest diverging lineage has to be found among the Cotulinae, the Osmitopsidinae and the clade of Inulanthera and Ursinia.
Fig. 1.
Phylogeny (gene tree) of Compositae–Anthemideae based on combined cpDNA sequences (ndhF, trnL-trnF) with subtribal assignment according to Oberprieler & al. (2007, 2019), Sonboli & Oberprieler (2010) and Sonboli & al. (2012). Clade support values (posterior probabilities > 0.9) are indicated.
Fig. 2.
Phylogeny (gene tree) of Compositae–Anthemideae based on combined nrDNA sequences (ITS1, 5.8S, ITS2) with subtribal assignment according to Oberprieler & al. (2007, 2019), Sonboli & Oberprieler (2010) and Sonboli & al. (2012). Clade support values (posterior probabilities > 0.9) are indicated.
In general, support values of monophyletic groups appear to be much higher in the analyses of concatenated sequences (Fig. 3) than in the coalescent-based species-tree reconstruction (Fig. 4). Owing to the comprehensive topological correspondence observed between the plastid phylogeny (Fig. 1) and the tree reconstruction based on nrDNA ITS (Fig. 2), we think that this is a consequence of the incongruence among the three single-copy nuclear markers ( Online Fig. S1 (wi.52.52108_OnlineFig_S1.pdf)– S3 (wi.52.52108_OnlineFig_S3.pdf)), which has led to the diminishing posterior probabilities in the coalescent-based reconstruction (Fig. 4), while in the concatenated analysis (Fig. 3) these information-poor and contradicting markers are overridden by the more information-rich and less contradicting signals from cpDNA and nrDNA ITS.
Nevertheless, the subtribal classification in general and the affiliation of hitherto unassigned genera in particular receive support from both reconstructions in many cases: (1) the sister-group relationship between Ursinia (Ursiniinae) and Inulanthera; (2) the lack of support for the Athansiinae; (3) the monophyly of the Phymasperminae; (4) the monophyly of the Handeliinae; (5) the monophyly of the Artemisiinae including Hulteniella and Lepidolopha; (6) the monophyly of the Leucanthemopsidinae including Phalacrocarpum; (7) the monophyly of the Leucantheminae including Daveaua, Heteromera and Otospermum; (8) the monophyly of the Santolininae; (9) the monophyly of the Glebionidinae including Endopappus and Nivellea; (10) the sister-group relationship of the Anthemidinae and Matricariinae, but with the lack of support for the monophyly of both subtribes; and (11) the isolated positions of Brocchia, Lonas and Vogtia.
Fig. 3.
Phylogeny of Compositae–Anthemideae based on a species-tree reconstruction with concatenated plastid and nuclear markers (cpDNA ndhF, trnL-trnF; nrDNA ITS1-5.8S-ITS2, ETS; nDNA DSP, VIP5, NPF3.1). Subtribal assignment of genera according to Oberprieler & al. (2007, 2019), Sonboli & Oberprieler (2010) and Sonboli & al. (2012). Clade support values (posterior probabilities > 0.9) are indicated.
Fig. 4.
Phylogeny of Compositae–Anthemideae based on a coalescent-based species-tree reconstruction with plastid and nuclear markers (cpDNA ndhF, trnL-trnF; nrDNA ITS1-5.8S-ITS2, ETS; nDNA DSP, VIP5, NPF3.1). Subtribal assignment of genera according to Oberprieler & al. (2007, 2019), Sonboli & Oberprieler (2010) and Sonboli & al. (2012). Clade support values (posterior probabilities > 0.9) are indicated.
Discrepancy between the two species-tree reconstructions mostly concern (1) the Cotulinae (monophyletic in the concatenated, but not in the coalescent-based reconstruction); (2) the position of Osmitopsis (sister to the Cotulinae in the concatenated, but with unclear relationships in the coalescent-based analysis); (3) the monophyly of the Pentziinae (supported in the concatenated, but not in the coalescent-based analysis); (4) the sister-group relationship of Glebionidinae and Santolininae (supported in the concatenated, but not in the coalescent-based analysis); and (5) the monophyly of the Anthemidinae (supported in the concatenated, but not in the coalescent-based analysis).
Taxonomic consequences
The previously proposed subtribal classification of Compositae–Anthemideae (Oberprieler & al. 2007, 2009) was based on sequence information from nrDNA ITS and cpDNA ndhF for 103 and 62 species of the tribe, respectively, and resulted in the acknowledgement of 14 subtribes, but left a considerable number of genera unassigned to a subtribe due to missing sequence information or unresolved positions in the phylogenetic reconstructions. Our present contribution managed (at least for the most comprehensive tree based on nrDNA ITS sequence variation; Fig. 2) to include all presently accepted genera of the tribe with the exception of two unispecific ones, Ajaniopsis (from China and Tibet) and Cancriniella (C Asia). Enlargement of the taxonomic sampling for the mentioned molecular markers and addition of further sequence information from the chloroplast (trnL-trnF intergenic spacer region) and the nuclear genome (DSP, VIP5 and NPF3.1) allow us now to propose an updated subtribal classification of the Anthemideae, in which all of the genera with hitherto unsecure subtribal placement are either assigned to one of the already existing subtribes or form the basis of subtribes newly described. Our treatment presented here therefore consists of 19 subtribes that are arranged in grades or clades based on biogeographical patterns in the following. The description of subtribes is based on descriptions given in Oberprieler & al. (2007) but updated wherever required by a new circumscription.
New to science are the five unigeneric subtribes Brocchiinae, Inulantherinae, Lepidophorinae, Lonadinae and Vogtiinae. While the erection of four of these independent subtribes is the consequence of the isolated positions of Brocchia, Lepidophorum, Lonas and Vogtia in the phylogenetic reconstructions presented here, the constant and well-supported grouping of Inulanthera as sister to Ursinia would have also allowed inclusion of this orphan genus into Ursiniinae. However, we refrain from this assignment because of considerable morphological differences between the two genera, which would have made the resulting subtribe extremely diverse and lacking of predictive information. Inulanthera differs from Ursinia most distinctly by the possession of basally caudate anthers; a character expression that is shared in the whole tribe only by the genera Osmitopsis (subtribe Osmitopsidinae) and Hippolytia (subtribe Artemisiinae). Additionally, the densely arranged, discoid capitula (laxly arranged and mostly radiate in Ursinia) and the achenes with a corona of small, entire to toothed scales terminating each rib (in contrast to the uni- or biseriate pappus exhibited by Ursinia) argue for acceptance of an independent subtribe Inulantherinae.
I. Southern hemisphere grade
1. Osmitopsidinae Oberpr. & Himmelr. in Willdenowia 37: 94. 2007. – Type: Osmitopsis Cass. (Osmitopsis asteriscoides (L.) Less.).
Description — Shrubs or subshrubs. Indumentum absent or of basifixed hairs. Leaves alternate, entire to lobed. Capitula solitary or in lax corymbs, radiate. Involucre campanulate. Phyllaries in 2–4 rows, often with scarious margins. Receptacle flat to conic, paleate; paleae narrowly elliptic to obovate, canaliculate and enclosing florets. Ray florets female or neuter; limb white, occasionally pilose abaxially, tube occasionally pilose. Disc florets hermaphrodite or male; corolla 5-lobed, yellow; anthers basally caudate, with non-polarized endothecial tissue and a slender filament collar; stylopodium sometimes large and persistent in fruit. Achenes obovoid to ellipsoid, 3- or 4-angled or -ribbed; apex with a corona of subulate to triangular, basally fused scales or marginally rounded. Embryo sac development unknown. Base chromosome number x = 10.
Distribution — South Africa.
Members — Osmitopsis Cass. (9).
Notes — The isolated position of the genus in the tribe already mentioned by Bremer (1972) and Nordenstam (1987) and acknowledged by classification in a unigeneric subtribe by Oberprieler & al. (2007) is unequivocally supported by the present phylogenetic reconstructions. The similarity with Inulanthera (subtribe Inulantherinae) and Hippolytia (Artemisiinae) due to the possession of basally caudate anthers does not correspond to a close evolutionary relationship to these genera.
2. Cotulinae Kitt., Taschenb. Fl. Deutschl., ed. 2, 2: 609. 1844. – Type: Cotula L. (Cotula coronopifolia L.).
= Thaminophyllinae K. Bremer & Humphries in Bull. Nat. Hist. Mus. London, Bot. 23: 144. 1993. – Type: Thaminophyllum Harv. (Thaminophyllum mundtii Harv.).
Description — Shrubs, subshrubs, perennial or annual herbs (Cotula, Leptinella, Soliva). Indumentum of basifixed hairs or absent. Leaves alternate or opposite, entire, lobed, pinnatifid to 1- or 2-pinnatisect. Capitula solitary or in lax to dense corymbs, radiate, disciform or discoid. Involucre broadly campanulate, hemispheric to cylindric or obconic, sometimes (Leptinella) umbonate. Phyllaries in 2–4 rows, without (Lidbeckia) or with narrow to broad scarious margins, sometimes (Cotula) with central resin ducts. Receptacle flat to hemispheric or conic, glabrous or hairy (Lidbeckia, Thaminophyllum), epaleate or with few marginal paleae (Schistostephium). Ray florets and outer disc florets (when present) female, rarely sterile or neuter (Lidbeckia), sometimes stalked (Cotula); limb white or yellow, rarely pilose (Inezia), sometimes confluent with achene and tube short or absent (Adenanthellum, Inezia, Thaminophyllum). Disc florets hermaphrodite or functionally male (Hippia, Leptinella, Schistostephium, Soliva); corolla 3-, 4- or sometimes 5-lobed (Adenanthellum, Hippia); anthers with non-polarized endothecial tissue and a slender filament collar; stylopodium sometimes large and persistent in fruit (Lidbeckia, Thaminophyllum). Achenes oblong to obovoid, terete with 2 or 3 adaxial or 3–10 ribs, sometimes 3- or 4-angled, often dorsiventrally compressed with 2 lateral, wing-like ribs; apex truncate or marginally rounded, ecoronate, rarely with minute scales (Inezia); pericarp with or without myxogenic cells and/or resin canals in ribs, sometimes papillose or hairy (Cotula, Hippia). Embryo sac development monosporic (only known in Cotula). Base chromosome numbers x = 8, 9, 10, 13.
Distribution — S and E Africa, Australia, New Guinea, New Zealand, South America, S oceanic islands; some species widespread and naturalized as weeds.
Members — Adenanthellum B. Nord. (1), Cotula L. (58), Hilliardia B. Nord. (1), Hippia L. (8), Inezia E. Phillips (2), Leptinella Cass. (33), Lidbeckia P. J. Bergius (3), Schistostephium Less. (12), Soliva Ruiz & Pav. (8), Thaminophyllum Harv. (3).
Notes — The circumscription of this subtribe with its ten genera proposed by Oberprieler & al. (2007) is corroborated by all present phylogenetic reconstructions except the coalescent-based species-tree reconstruction (Fig. 4), where Hippia is associated with members of subtribe Pentziinae. Since this position and the reciprocal monophyly of each of both subtribes (Cotulinae and Pentziinae) is not supported by posterior probabilities, we think that any hypothesis of a non-monophyly of the subtribe is unsubstantiated. Species numbers given for Cotula and Leptinella are only approximations due to the lack of recent and/or comprehensive revisions of the two genera (Leptinella: Lloyd & Webb 1987; Himmelreich & al. 2012, 2014; Cotula: Powell & al. 2014; Jakoet & al. 2019).
3. Ursiniinae K. Bremer & Humphries in Bull. Nat. Hist. Mus. London, Bot. 23: 91. 1993. – Type: Ursinia Gaertn. (Ursinia paradoxa (L.) Gaertn.).
Description — Annual or perennial herbs or shrublets. Indumentum absent or of basifixed hairs. Leaves alternate, entire to 2-pinnatisect, sometimes succulent. Capitula solitary or in lax corymbs, radiate or discoid, pedunculate. Involucre hemispheric. Phyllaries in 3–7 rows, with narrow to broad scarious margins. Receptacle hemispheric, paleate; paleae canaliculate, elliptic or narrowly linear with an apical limb. Ray florets usually neuter, sometimes female and fertile; limb yellow, orange, white or reddish. Disc florets hermaphrodite, fertile; corolla 5-lobed, yellow, purplish. Achenes cylindric or obovoid, straight or curved, circular in cross-section, with 5 ribs and a basal tuft of hairs or glabrous; apex with a uniseriate pappus of 5–10 ovate or circular scales, a biseriate pappus of 5 outer such scales and 5 inner subulate ones or rarely epappose; pericarp rarely with myxogenic cells. Embryo sac development monosporic. Base chromosome numbers x = 5, 7, 8.
Distribution — South Africa, Namibia, Botswana, Ethiopia.
Members — Ursinia Gaertn. (43).
Notes — The present results support our previous findings (Oberprieler & al. 2007) that the circumscription of Ursiniinae sensu Bremer & Humphries (1993) with the inclusion of genera classified in subtribes Athanasiinae (Athanasia, Hymenolepis, Lasiospermum) and Phymasperminae (Eumorphia, Gymnopentzia, Phymaspermum) is not supported as a monophyletic assemblage. Conversely, all gene- and species-tree reconstructions unequivocally indicate the close phylogenetic relationship with the S African genus Inulanthera. However, due to the considerable morphological differences between Ursinia and Inulanthera described in detail in the following subtribal account, we have refrained from uniting the two genera in Ursiniinae. A preliminary molecular phylogenetic study of Ursinia by Swelankomo (2008) based on nrDNA ITS sequence information revealed some support for the infrageneric classification of Ursinia species into U. subg. Ursinia (with a biseriate pappus of five outer scales and five inner subulate awns) and U. subg. Sphenogyne (Aiton) Prassler (with a uniseriate pappus of 5–10 ovate or circular scales) but did not provide any justification for the acknowledgement of the two monophyletic groups as independent genera. As a consequence, four newly discovered species of this plant group were all described in the broadly circumscribed genus Ursinia (Magee & al. 2014).
4. Inulantherinae Oberpr. & Töpfer, subtrib. nov.
Type: Inulanthera Källersjö (Inulanthera calva (Hutch.) Källersjö).
Description — Shrubs or subshrubs. Indumentum absent or of basifixed hairs. Leaves alternate, entire to lobed. Capitula in dense corymbs, discoid. Involucre hemispheric to spheric. Phyllaries in 3 rows, with narrow, pale to light brown scarious margins. Receptacle flat, paleate, rarely epaleate; paleae linear, flat to shallowly canaliculate, with a central resin duct. Florets hermaphrodite, fertile; corolla 5-lobed, yellow; anthers basally caudate, with polarized endothecial tissue. Achenes obovoid, circular in cross-section, with (8–)10 ribs; apex with a corona of small, entire to toothed scales terminating each rib; pericarp smooth, sometimes papillose, without myxogenic cells or resin sacs, but with protruding, light brown glands. Embryo sac development and base chromosome number unknown.
Distribution — South Africa, Swaziland, Lesotho, Angola, Zimbabwe, Madagascar.
Members — Inulanthera Källersjö (9; see Magoswana & al. 2016).
Notes — A close evolutionary relationship between Inulanthera and the two genera Gonospermum Less. and Lugoa DC. from the Canary Islands was suggested by the treatment of these genera under a subtribe Gonosperminae (Bremer & Humphries 1993) but was demonstrated as being unsupported in molecular phylogenetic analyses (Oberprieler & al. 2007, 2009; Sonboli & al. 2012), hence the subtribal placement of Inulanthera remained unresolved. Despite the consistent sister-group relationship of Inulanthera and Ursinia in the previously mentioned and present molecular phylogenetic studies, distinct differences between the two genera in morphological respects rather suggest the erection of an independent, unigeneric subtribe than the merging of the two genera into an extremely heterogeneous one: Inulanthera differs from Ursinia by its discoid capitula in dense corymbs, its caudate anthers and its achenes devoid of a well-developed, scaly pappus. Within the whole tribe, the caudate anthers are shared only by Osmitopsis (Osmitopsidinae) and Hippolytia (Artemisiinae; Oberprieler & al. 2007, 2009), but close phylogenetic relationships to these three genera have never been substantiated.
5. Athanasiinae Pfeiff., Nomencl. Bot. 1: 323. 1872. – Type: Athanasia L. (Athanasia crithmifolia (L.) L.).
Description — Shrubs or shrublets, rarely perennial to annual herbs (Adenoglossa, Lasiospermum). Indumentum absent or of basifixed or stellate (Athanasia, Hymenolepis) hairs. Leaves alternate or opposite, entire or lobed to pinnatifid or 1- or 2-pinnatisect. Capitula solitary or in lax to dense corymbs, radiate, disciform or discoid. Involucre hemispheric, spheric to urceolate. Phyllaries in 2–5 rows, without or with scarious margins, with central resin canals or sacs (in Eriocephalus in 2 unequal rows, outer phyllaries with very wide scarious margins, inner ones connate and hairy). Receptacle flat, hemispheric to conic, paleate or epaleate (Adenoglossa, Leucoptera); paleae flat or canaliculate, rarely villous (Eriocephalus). Ray florets female; limb yellow, white or reddish. Disc florets hermaphrodite (male in Eriocephalus); corolla 5-lobed; tube sometimes with long stalked hairs (Athanasia); anthers with polarized endothecial tissue, rarely non-polarized (Eriocephalus), and a slender filament collar. Achenes cylindric to obovate, either terete and with 5–12(–18) ribs or dorsiventrally flattened and laterally winged (Adenoglossa, Leucoptera); apex marginally rounded, with a short, thickened rim (Athanasia) or with a corona or scales (Adenoglossa, Hymenolepis, Leucoptera); pericarp glabrous or densely hairy (Eriocephalus, Lasiospermum), with or without myxogenic cells and/or resin sacs. Embryo sac development monosporic (only known in Lasiospermum). Base chromosome number x = 8, 9.
Distribution — South Africa, Namibia, Botswana, Lesotho, Egypt (Sinai), Israel, Jordan.
Members — Adenoglossa B. Nord. (1), Athanasia L. (41), Eriocephalus L. (32), Hymenolepis Cass. (7), Lasiospermum Lag. (4), Leucoptera B. Nord. (3).
Notes — The subtribe Athanasiinae in its present circumscription is surely the most problematic generic assemblage in the subtribal classification of the tribe presented here. The present circumscription corresponds completely with the one proposed in our former treatment (Oberprieler & al. 2007, 2009), where its non-monophyletic nature was discussed to some extent. Our present phylogenetic reconstructions do not support a monophyly of the Athanasiinae—neither the gene trees with representatives of all six mentioned genera (Fig. 1, 2) nor the species trees with the reduced set of those four genera, for which a complete data matrix was achieved (Fig. 3, 4). This is paralleled by the quite diverse morphological circumscription of the subtribe in itself. Nevertheless, we presently refrain from a decomposition of this possibly paraphyletic subtribe until a more complete sampling and a more reliable phylogenetic reconstruction is available. Species numbers of the present account were updated following taxonomic work done by Powell & Magee (2013) in Athanasia and by Magoswana & Magee (2014) and Magoswana & al. (2015) in Hymenolepis.
6. Phymasperminae Oberpr. & Himmelr. in Willdenowia 37: 99. 2007. – Type: Phymaspermum Less. (Phymaspermum junceum Less.).
Description — Shrubs or shrublets. Indumentum absent or of basifixed hairs. Leaves opposite or alternate, entire to lobed. Capitula solitary or in lax corymbs, radiate or discoid. Involucre hemispheric to spheric, rarely cylindric to obconic. Phyllaries in 2–4 rows, with scarious, sometimes ciliate margins. Receptacle flat to conic, epaleate, sometimes paleate (Eumorphia, occasionally in Gymnopentzia); paleae linear canaliculate. Ray florets female; limb white, yellow or purplish. Disc florets hermaphrodite; corolla 5-lobed; anthers with polarized endothecial tissue and a slender filament collar. Achenes cylindric or ellipsoid, terete with 10–12(–18) ribs; apex truncate or with an entire to dentate, thickened rim or corona; pericarp papillose, without myxogenic cells or resin sacs (in Phymaspermum with ovoid myxogenic trichomes and resin sacs in some of ribs). Embryo sac development and base chromosome number unknown.
Distribution — South Africa, Lesotho, Swaziland, Zimbabwe, Namibia.
Members — Eumorphia DC. (6), Gymnopentzia Benth. (1), Phymaspermum Less. (17).
Notes — Apart from the strange but unsupported position of one of its members (i.e. Phymaspermum) in the cpDNA gene tree (Fig. 1), the monophyly of this subtribe is corroborated by the other phylogenetic reconstructions (Fig. 2, 3, 4). Closer relationships appear to exist with the Athanasiinae, with which the Phymasperminae share the possession of anthers with polarized endothecial tissue and a slender filament collar. However, since even inclusion of its three members into a broader circumscribed Athanasiinae would not make the latter subtribe monophyletic, we suggest keeping this small generic assemblage in a subtribe of its own. Revisionary work done by Swelankomo (2011) for Eumorphia and Ruiters & al. (2016) for Phymaspermum updated the species numbers given in the present account.
II. Asian-southern African grade
7. Pentziinae Oberpr. & Himmelr. in Willdenowia 37: 99. 2007. – Type: Pentzia Thunb. (Pentzia crenata Thunb., nom. illeg.).
Description — Shrubs, subshrubs or perennial to annual herbs. Indumentum of basifixed hairs or absent, rarely of medifixed hairs (Pentzia). Leaves alternate or rarely opposite (Pentzia, Rennera), entire, lobed or 1- or 2-pin-natisect. Capitula solitary or in corymbs, rarely closely aggregated (Marasmodes), discoid or disciform, sometimes radiate (Cymbopappus, Foveolina, Oncosiphon). Involucre hemispheric to cylindric, sometimes urceolate (Marasmodes). Phyllaries in 3–5 rows, with or without scarious margins. Receptacle flat or convex to conic, epaleate. Ray florets female; limb white or pinkish. Disc florets hermaphrodite; corolla 4- or 5-lobed, sometimes tube swollen and brittle (Oncosiphon) or with thick vascular strands (Cymbopappus, Marasmodes, Pentzia); anthers with non-polarized endothecial tissue and a slender filament collar. Achenes oblong to obovoid, with 4- or 5 ribs, sometimes triquetrous in cross-section and with 1 adaxial and 2 lateral ribs (Myxopappus); apex marginally rounded, with an entire or toothed rim, an oblique, adaxially longer, entire corona, a corona of 3–10 scales or with a large adaxial and a smaller abaxial scale; pericarp sometimes spongy (Myxopappus), with myxogenic cells on ribs and abaxial surface, without resin sacs, rarely without myxogenic cells (Oncosiphon, Rennera). Embryo sac development monosporic (only known in Oncosiphon). Base chromosome number x = 6, 7, 8, 9.
Distribution — South Africa, Lesotho, Namibia, Botswana, Morocco, Algeria, Chad, Somalia, Yemen.
Members — Cymbopappus B. Nord. (3), Foveolina Källersjö (5), Marasmodes DC. (13), Myxopappus Källersjö (2), Oncosiphon Källersjö (8), Pentzia Thunb. (27, incl. Rennera Merxm.).
Notes — While in the analysis based on concatenated sequences the subtribe Pentziinae received strong support for being monophyletic (Fig. 3), this signal is less clear in the other phylogenetic reconstructions. In the tree based on cpDNA sequence variation, a monophyletic Pentziinae is found comprising also the representative of Mausolea from the Artemisiinae (Fig. 1), while in the nrDNA tree (Fig. 2) only a group excluding Myxopappus receives strong support, and in the coalescent-based species tree (Fig. 4) a strongly supported relationship with subtribe Cotulinae emerged. These equivocal circumscriptions and relationships may be a consequence of either hybridization events or incomplete lineage sorting connected with the intermediary role of the Pentziinae in biogeographical respects between the S hemisphere-based subtribes on the one hand and the Asian-based subtribes Artemisiinae and Handeliinae on the other. This is additionally supported by the occurrence of some species of Pentzia in N Africa and SW Asia (Oberprieler & al. 2007).
Delimitation of genera in the Pentziinae is highly problematic. Phylogenetic analyses based on nrDNA ITS and cpDNA markers by Magee & al. (2015) revealed considerable discrepancies between tree topologies based on the two datasets with little support for the monophyly of the hitherto accepted genera; exceptions being Marasomodes (well supported by both datasets), Myxopappus (supported in the cpDNA tree) and Rennera (well supported by both datasets but nested in a paraphyletic genus Pentzia). Except for the transfer of the four Rennera species to Pentzia proposed by Magee & al. (2015), no further nomenclatural consequences were drawn from the mentioned analyses, and a further discussion of generic limits in this subtribe must await more comprehensive genetic/genomic datasets and analyses. However, due to the extremely productive revisionary work of A. R. Magee (Compton Herbarium, Cape Town, South Africa) and his collaborators, the taxonomy of some genera is now well understood (Marasmodes, Magee & al. 2017; Oncosiphon, Kolokoto & Magee 2018; the Pentzia incana group, Magee & Tilney 2012).
8. Handeliinae K. Bremer & Humphries in Bull. Nat. Hist. Mus. London, Bot. 23: 108. 1993. – Type: Handelia Heimerl (Handelia trichophylla (Schrenk) Heimerl).
= Cancriniinae K. Bremer & Humphries in Bull. Nat. Hist. Mus. London, Bot. 23: 96. 1993. – Type: Cancrinia Kar. & Kir. (Cancrinia chrysocephala Kar. & Kir.).
Description — Subshrubs or annual, biennial (hapaxanthic) or perennial (pollacanthic) herbs. Indumentum absent or of basifixed, rarely of medifixed hairs (some species of Tanacetopsis and Xylanthemum). Leaves alternate, lobed or apically trifid, 1- or 2-pinnatipartite to 3- or 4-pinnatisect. Capitula solitary, in lax to dense corymbs or in a long panicle (Lepidolopsis), discoid or radiate. Involucre hemispheric to spheric or obconic (Trichanthemis), sometimes umbonate (Sclerorhachis). Phyllaries in 2–4(or 5) rows, with narrow to broad scarious margins. Receptacle hemispheric, epaleate or paleate (Handelia, Sclerorhachis); paleae subulate to linear, flat to canaliculate, sometimes readily deciduous (Sclerorhachis). Ray florets female or neuter; limb white, yellow, pink or violet. Disc florets hermaphrodite; corolla 5-lobed, sometimes 4–6-lobed (Lepidolopsis), sometimes hairy (Tanacetopsis, Trichanthemis); anthers with non-polarized endothecial tissue and a balusterform filament collar (slender in Allardia and some Tanacetopsis species). Achenes cylindric to obconic, circular to elliptic in cross-section, with 4–10(–15) ribs, sometimes with 3–5 adaxially arranged ribs (Microcephala); apex with a corona formed by 5–20 (Cancrinia, Ugamia) or 25–50 bristle-like scales (Allardia), a short rim or of laciniate scales of various shapes, rarely ecoronate (Pseudohandelia, Sclerorhachis); pericarp with or without myxogenic cells, without resin sacs, glabrous or rarely sparsely to densely hairy (Allardia, Cancrinia, Trichanthemis, Ugamia). Embryo sac development unknown. Base chromosome number x = 7 (Microcephala), 9.
Distribution — Iran, Afghanistan, Pakistan, C Asia, Mongolia, China.
Members — Allardia Decne. (4), Cancrinia Kar. & Kir. (4), Cancriniella Tzvelev (1), Handelia Heimerl (1), Lepidolopsis Poljakov (1), Microcephala Pobed. (5), Polychrysum (Tzvelev) Kovalevsk. (1), Pseudohandelia Tzvelev (1), Richteria Kar. & Kir. (6), Sclerorhachis (Rech. f.) Rech. f. (4), Tanacetopsis (Tzvelev) Kovalevsk. (21), Trichanthemis Regel & Schmalh. (9), Ugamia Pavlov (1), Waldheimia Kar. & Kir. (4).
Notes — The phylogeny of the subtribe was studied in detail by Oberprieler & al. (2019) in a multi-locus approach based on both plastid and nuclear markers. Incongruence among the marker-wise gene-tree reconstructions was interpreted there as a result of ample hybridization having occurred in the evolutionary history of the members of Handeliinae. While generic circumscriptions were unaddressed by the mentioned study due to the limited sampling of representatives from the species-rich genera, the exclusion of Xylanthemum from the subtribe and its transfer to Anthemidinae as proposed earlier by Sonboli & al. (2012) and the polyphyly of Allardia and its classification as two independent genera (Allardia and Waldheimia) received good support from these phylogenetic reconstructions. There is still a lack of information for the subtribal placement of the unispecific genus Cancriniella Tzvelev. However, the close relationship to Cancrinia and Trichanthemis karataviensis (the type of Trichanthemis), as proposed by Poljakov (1959) by uniting them under a more comprehensive genus Cancrinia, argues for the classification of Cancriniella in Handeliinae and awaits support from a molecular phylogenetic analysis of this C Asian endemic.
9. Artemisiinae Less. in Linnaea 5: 163. 1830. – Type: Artemisia L. (Artemisia vulgaris L.).
= Chrysantheminae Less. in Linnaea 6: 167. 1831. – Type: Chrysanthemum L. (Chrysanthemum indicum L., typ. cons.).
Description — Shrubs, subshrubs, perennial or annual herbs, sometimes with basally woody, virgate and sometimes leafless stems (Lepidolopha). Indumentum absent, of basifixed or medifixed (sometimes stellate) hairs. Leaves rosulate or alternate, entire, lobed, serrate to 1–3-pinnatisect. Capitula solitary, in lax to dense corymbs or in panicles, rarely in dense glomerules (Turaniphytum), radiate, disciform or discoid. Involucre hemispheric to cylindric, obconic or urceolate. Phyllaries in 1–7 rows, with narrow to broad scarious margins. Receptacle flat to conic, epaleate or paleate, sometimes pilose. Ray florets (when present) female or neuter; limb white, yellow or pink. Outer disc florets (in disciform capitula) female, corolla absent or slender, 2- or 3(–5)-lobed. Central disc florets hermaphrodite or male (rarely neuter); corolla (4 or)5-lobed; anthers basally rounded, rarely caudate (Hippolytia), with non-polarized endothecial tissue and a slender filament collar. Achenes ellipsoid to obovoid without or with 3–8(–12) ribs, sometimes flattened; apex marginally rounded, sometimes with a rounded rim (Artemisiella, Hippolytia, Hulteniella), a lacerate corona with small scales (Crossostephium, Nipponanthemum, Opisthopappus, Spheromeria) or a corona formed by 8–10 linear-elliptic scales (Lepidolopha); pericarp with or without myxogenic cells in rows, without resin sacs (with longitudinal resin canals in Hippolytia), sometimes pilose. Embryo sac development monosporic (only known in Arctanthemum, Artemisia and Chrysanthemum). Base chromosome number x = 6, 7, 8, 9, 10, 11, 17.
Distribution — Worldwide, with a centre of diversity in C Asia.
Members — Ajania Poljakov (39), Ajaniopsis C. Shih (1), Arctanthemum (Tzvelev) Tzvelev (3), Artemisia L. (522, incl. Seriphidium Fourr.), Artemisiella Ghafoor (1), Brachanthemum DC. (10), Chrysanthemum L. (37), Crossostephium Less. (1), Elachanthemum Y. Ling & Y. R. Ling (1), Filifolium Kitam. (1), Hippolytia Poljakov (19), Hulteniella Tzvelev (1), Kaschgaria Poljakov (2), Lepidolopha C. Winkl. (9), Leucanthemella Tzvelev (2), Mausolea Poljakov (1), Neopallasia Poljakov (3), Nipponanthemum Kitam. (1), Opisthopappus C. Shih (2), Phaeostigma Muldashev (3), Picrothamnus Nutt. (1), Sphaeromeria Nutt. (9), Stilpnolepis Krasch. (1), Tridactylina (DC.) Sch. Bip. (1) Turaniphytum Poljakov (2).
Notes — As in the previous subtribe, delimitation of genera in this extremely species-rich subtribe was beyond the aims of the present study. However, representatives of all mentioned 24 genera were found forming a strongly supported monophyletic group in the nrDNA ITS tree (Fig. 2). The subtribal circumscription and the inclusion of the formerly unassigned genus Lepidolopha was additionally supported both by the multi-locus analysis of Oberprieler & al. (2019) and the species-tree reconstructions presented here (Fig. 3, 4). The unispecific genus Ajaniopsis C. Shih, endemic to Tibet and China, still lacks a phylogeny-based subtribal classification. However, as discussed by Bremer & Humphries (1993) based on morphological evidence, membership of this annual in the Artemisiinae is beyond doubt.
III. Eurasian grade
10. Brocchiinae Oberpr. & Töpfer, subtrib. nov.
Type: Brocchia Vis. (Brocchia cinerea (Delile) Vis.).
Description — Annual herbs. Indumentum of basifixed hairs. Leaves alternate, pinnatipartite to pinnatisect, sometimes entire to lobed. Capitula solitary or in lax corymbs, discoid, pedunculate. Involucre hemispheric. Phyllaries in 2 rows, with narrow, pale membranous margins. Receptacle hemispheric to conic, epaleate. Disc florets hermaphrodite, fertile; corolla yellow, apically 4-lobed. Achenes obovoid, circular in cross-section, with c. 4 inconspicuous lateral and adaxial ribs; apex slanting, marginally rounded; pericarp with large, elongated myxogenic cells, without resin sacs. Embryo sac development unknown. Base chromosome number x = 9.
Distribution — N Africa, SW Asia.
Members — Brocchia Vis. (1).
Notes — As discussed in detail by Oberprieler (2004a), there are a number of morphological, anatomical and cytological characters that argue against the close relationship of Brocchia cinerea with Cotula, in which this primarily N African species was described by Delile (1813). The superficial similarity with Cotula due to the 4-merous disc florets is paralleled both by a number of other genera from Cotulinae (Hilliardia, Inezia, Leptinella, Lidbeckia, Schistostephium, Soliva, Thaminophyllum), but also from Anthemidinae (Nananthea), Artemisiinae (Artemisiella, Filifolium, Phaeostigma), Handeliinae (Lepidolopsis), Matricariinae (Matricaria) and Pentziinae (Foveolina, Myxopappus, Oncosiphon). A close evolutionary relationship of Brocchia and any of those generic assemblages, however, is excluded by the present phylogenetic reconstructions (gene trees based on cpDNA, nrDNA ITS, nDNA NPF3.1, Fig. 1, 2, Online Fig. S3 (wi.52.52108_OnlineFig_S3.pdf); species trees, Fig. 3, 4) and the groupings seen with Matricaria in nDNA DSP ( Online Fig. S1 (wi.52.52108_OnlineFig_S1.pdf)) and Nananthea in nDNA VIP5 ( Online Fig. S2 (wi.52.52108_OnlineFig_S2.pdf)) are not supported by any significant posterior probability values.
11. Vogtiinae Oberpr. & Töpfer, subtrib. nov.
Type: Vogtia Oberpr. & Sonboli (Vogtia microphylla (DC.) Oberpr. & Sonboli).
Description — Annual herbs. Indumentum of long and slender, appressed, medifixed hairs mixed with sessile glands. Leaves alternate and in axillary fascicles, simple and linear-lanceolate to 1- or 2-pinnatisect. Capitula in dense corymbs with up to 40 capitula, shortly pedunculate to sessile, discoid. Involucre hemispheric. Phyllaries in 2 or 3 rows, with yellowish or whitish, scarious, apically rounded and reflexed or subacute margins. Receptacle epaleate. Disc florets hermaphrodite, fertile; corolla 4- or 5-lobed, yellow, basally not clasping top of achene. Anthers with pointed, triangular apical appendages; pollen of “Anthemis type” with distinct spines. Achenes obovoid, with 8–10 very thin and narrow ribs; apex with a very short corona of protruding ribs forming teeth, c. 0.1 mm; pericarp without myxogenic cells and without resin sacs or ducts. Testa epidermis of an epidermal type (i.e. with undulating anticlinal walls). Embryo sac development unknown. Base chromosome number x = 9.
Distribution — Europe (France, Spain, Portugal), N Africa (Morocco).
Members — Vogtia Oberpr. & Sonboli (2).
Notes — The genus Vogtia with its two members, V. annua and V. microphylla, was erected as a result of a phylogenetic analysis of the genus Tanacetum based on nrDNA ITS and cpDNA trnH-psbA sequence variation done by Sonboli & al. (2012), who found the latter of the two species consistently and significantly excluded from a clade formed by further members of Anthemidinae (Anthemis, Archanthemis, Cota, Nananthea, Tanacetum, Tripleurospermum, Xylanthemum) and Matricariinae (Achillea, Anacyclus, Heliocauta, Matricaria). Originally described as members of Tanacetum, the two species are distinctly deviating from all other species of this genus by their annual life form. The unique phylogenetic position of Vogtia corroborated by the present gene- and species-tree reconstructions is morphologically supported by the pointed apical appendages of the anthers and the testa epidermis with undulating anticlinal walls. While the latter is unique in the whole tribe, the former is observed in all members of Artemisiinae, “though variously expressed” (Bremer & Humphries 1993).
12. Matricariinae Willk. in Willkomm & Lange, Prodr. Fl. Hispan. 2: 92. 1870. – Type: Matricaria L. (Matricaria recutita L., typ. cons.).
= Achilleinae K. Bremer & Humphries in Bull. Nat. Hist. Mus. London, Bot. 23: 126. 1993. – Type: Achillea L. (Achillea millefolium L.).
Description — Subshrubs or perennial or annual herbs. Indumentum of basifixed, sometimes asymmetrically medifixed (Achillea) hairs. Leaves alternate or in a basal rosette (Heliocauta), rarely entire, usually dentate to 4-pinnatisect, sometimes vermiform. Capitula solitary or in lax to dense corymbs, radiate, disciform or discoid. Involucre hemispheric to cylindric or obconic. Phyllaries in 2 or 3 rows, with narrow to broad scarious margins. Receptacle flat, hemispheric or conic, paleate or epaleate (Matricaria); paleae flat to convex or canaliculate. Ray florets female; limb white, yellow or pink; tube ± flattened. Disc florets hermaphrodite; corolla (4 or)5-lobed, basally ± saccate and clasping top of achene; anthers with non-polarized endothecial tissue and a balusterform filament collar. Achenes obovoid, terete with 3–5 weak ribs or dorsiventrally flattened and with 2 lateral ribs or wings; apex marginally rounded or with a narrow marginal corona (Anacyclus, Matricaria); pericarp with or without myxogenic cells, sometimes with longitudinal resin ducts (Achillea, Heliocauta). Embryo sac development monosporic. Base chromosome number x = 9.
Distribution — Europe, Asia, N Africa, W North America.
Members — Achillea L. (115), [incl. Leucocyclus Boiss. (1), Otanthus Hoffmanns. & Link (1), see Guo & al. (2004), Ehrendorfer & Guo (2005, 2006)], Anacyclus L. (9), Heliocauta Humphries (1), Matricaria L. (6).
Notes — The reciprocal monophyly of the two closely related subtribes Anthemidinae and Matricariinae is not supported by our present analyses. Only when Matricaria is excluded from both subtribes do they receive strong support in the phylogenetic reconstruction based on concatenated sequence information (Fig. 3). As discussed earlier (Oberprieler & al. 2007), the main difference between the two subtribes is found in the embryo sac development, which follows a monosporic type in Matricariinae and a tetrasporic one in Anthemidinae. Since a tetrasporic embryo sac development constitutes an apomorphic condition in the otherwise monosporic tribe (with exceptions in Argyranthemum and Heteranthemis in the Glebionidinae), we cannot exclude the possibility that a monophyletic subtribe Anthemidinae is nested in a paraphyletic Matricariinae. This situation already described in Oberprieler & al. (2007) based on nrDNA ITS sequence information has not been resolved by adding more markers in the present analysis. However, we still refrain from uniting these two embryologically well-separated generic assemblages without an unequivocal phylogenetic signal.
In contrast to former enumerations, the genus Anacyclus has been reduced in its species number due to the transfer of three species to the genus Cota in the Anthemidinae (Vitales & al. 2018). Both genera share the character of dorsi-ventrally flattened achenes, but the mentioned sequence-based phylogenetic analysis (nrDNA ITS, cpDNA psbA-trnH) revealed that the three E Mediterranean representatives, A. anatolicus, A. latealatus and A. nigellifolius, do not belong to the W Mediterranean lineage of Anacyclus.
13. Anthemidinae Dumort., Fl. Belg.: 69. 1827. – Type: Anthemis L. (Anthemis arvensis L.).
= Pyrethrinae Horan., Char. Ess. Fam.: 90. 1847. – Type: Pyrethrum Zinn. (Pyrethrum corymbosum (L.) Willd.).
= Gonosperminae K. Bremer & Humphries in Bull. Nat. Hist. Mus. London, Bot. 23: 106. 1993. – Type: Gonospermum Less. (Gonospermum fruticosum Less.).
= Tanacetinae K. Bremer & Humphries in Bull. Nat. Hist. Mus. London, Bot. 23: 99. 1993. – Type: Tanacetum L. (Tanacetum vulgare L.).
Description — Subshrubs, short- to long-lived perennial herbs, biennials or annuals; sometimes shrublets with basally woody, virgate and sometimes leafless stems (Xylanthemum). Indumentum absent or of medifixed and/or basifixed (Tanacetum, Tripleurospermum) hairs. Leaves alternate, dentate to lobed or 1–3-pinnatisect. Capitula solitary or in lax to dense corymbs, radiate, disciform or discoid. Involucre hemispheric or obconic, sometimes umbonate. Phyllaries in 1–5 rows, with scarious margins. Receptacle hemispheric or conic, paleate or epaliate; paleae flat, sometimes subulate (Anthemis). Ray florets female or neuter; limb white, yellow or pink; tube sometimes hairy. Disc florets hermaphrodite; corolla 5-lobed, rarely 4-lobed (Nananthea), sometimes hairy (Xylanthemum); anthers with non-polarized endothecial tissue and a balusterform filament collar. Achenes obovoid to obconic, circular in cross-section, with 5–10(–15) ribs or dorsiventrally flattened with 2 lateral ribs and 3–10 ribs on each surface (Cota), sometimes triquetrous and with 3(–5) ribs (Tripleurospermum); apex with a corona or auricle, sometimes ecoronate and/or marginally rounded, sometimes (Xylanthemum) with 3–6 adaxial, elliptic scales shorter than achene body; pericarp with myxogenic cells, sometimes without (Tanacetum), usually without resin sac or ducts, in Tripleurospermum with (1 or)2(–5) abaxial-apical resin sacs. Embryo sac development tetrasporic. Base chromosome number x = 9.
Distribution — Europe, SW Asia, N and E Africa, Canary Islands, North America.
Members — Anthemis L. (175), Archanthemis Lo Presti & Oberpr. (4), Cota J. Gay (43), Nananthea DC. (1), Tanacetum L. (154) [incl. Gonospermum Less. (4), Lugoa DC. (1), see Sonboli & al. (2012)], Tripleurospermum Sch. Bip. (40), Xylanthemum Tzvelev (8).
Notes — The subtribe received a new circumscription due to the establishment of the genus Archanthemis for four phylogenetically deviating Anthemis species (Lo Presti & al. 2010) and the transfer of the genus Xylanthemum from Handeliinae to Anthemidinae (Sonboli & al. 2012; Oberprieler & al. 2019). Following the phylogenetic analyses by Sonboli & al. (2012) based on nrDNA ITS and cpDNA trnH-psbA sequence information, Xylanthemum could even be sunk into synonymy with Tanacetum (like the two Canarian genera Gonospermum and Lugoa), but this must await a better-resolved molecular phylogeny of the latter genus.
As discussed under subtribe Matricariinae, the close relationship of Anthemidinae and Matricariinae is consistently supported by our present analyses. However, their reciprocal monophyly is questionable and their classification as two subtribes is only supported by a differing embryo sac development realized by those representatives surveyed for this character.
As representative of the genus Xylanthemum, we included a specimen labelled “Xylanthemum paradoxum” by Podlech, who never validly published that name when including Xylanthemum into Tanacetum (due to the existence of the older homonym T. paradoxum Bornm.) but described the species as T. paleaceum Podlech in his treatment of Compositae–Anthemideae in Flora iranica (Podlech 1986). Sonboli & al. (2012) demonstrated that T. paleaceum is closely related with the type of Xylanthemum (i.e. X. fisherae (Aitch. & Hemsl.) Tzvelev), but refrained from proposing a new combination due to uncertainties connected with the demarcation of Xylanthemum against Tanacetum. However, in order to accommodate Xylanthemum in the present subtribal classification, we herewith propose the new combination:
Xylanthemum paleaceum (Podlech) Oberpr. & Vogt, comb. nov. ≡ Tanacetum paleaceum Podlech in Rechinger, Fl. Iran. 158: 143. 1986.
14. Leucanthemopsidinae Oberpr. & Vogt in Willdenowia 37: 104. 2007. – Type: Leucanthemopsis (Giroux) Heywood (Leucanthemopsis alpina (L.) Heywood).
Description — Annual or perennial herbs. Indumentum of medifixed hairs. Leaves alternate or sometimes opposite (Phalacrocarpum), serrate-dentate to 1- or 2-pinnatisect. Capitula solitary, radiate. Involucre hemispheric. Phyllaries in 4 rows, with broad scarious margins. Receptacle convex, epaleate, sometimes hairy (Phalacrocarpum). Ray florets female or neuter; limb white or yellow, sometimes reddish (Phalacrocarpum). Disc florets hermaphrodite, rarely (Phalacrocarpum) functionally male; corolla 5-lobed; anthers with non-polarized endothecial tissue and a balusterform filament collar. Achenes obovoid, round in cross-section and with (3–)5–10 ribs, rarely dorsiventrally compressed and with 1 adaxial, 2 lateral and 2 abaxial ribs (Prolongoa); apex with a scarious corona or marginally rounded (Castrilanthemum, Phalacrocarpum); pericarp with myxogenic cells along ribs (without myxogenic cells in Phalacrocarpum), without resin sacs. Embryo sac development monosporic (only known in Leucanthemopsis). Base chromosome number x = 9.
Distribution — SW Europe, NW Africa.
Members — Castrilanthemum Vogt & Oberpr. (1), Hymenostemma Willk. (1), Leucanthemopsis (Giroux) Heywood (9), Phalacrocarpum (DC.) Willk. (1), Prolongoa Boiss. (1).
Notes — In contrast to the phylogenetic reconstructions based on nrDNA ITS (Fig. 2), both the gene tree based on plastid markers (Fig. 1) and the two species trees (Fig. 3, 4) strongly support the sister-group relationship of the Iberian endemic genus Phalacrocarpum and the closely knit generic assemblage of subtribe Leucanthemopsidinae. Tomasello & al. (2015) dated the divergence between Phalacrocarpum and the three other genera to c. 20 Ma and the further differentiation among the latter to the range between 7 Ma (divergence of Hymenostemma and Prologoa) and 17 Ma (divergence of Castilanthemum). Caused by the extremely long periods of evolutionary independence exhibited by the five lineages, the morphological diversity of the subtribe is considerable and gains even more heterogeneity by inclusion of Phalacrocarpum. However, erection of an independent, unigeneric subtribe for the latter genus would immediately question the treatment of the remaining genera as a single subtribal entity.
The infrageneric taxonomy of both the enigmatic Phalacrocarpum and the much younger genus Leucanthemopsis is complicated by evolutionary reticulations due to homoploid and polyploid hybrid speciation, respectively. Molecular-based analyses on species delimitations in the two genera were done by Criado Ruiz & al. (2021) and Tomasello & Oberprieler (submitted) and partially question the morphology-based taxonomic treatments proposed in Flora iberica (Pedrol 2019; Nieto Feliner 2019).
IV. Mediterranean clade
15. Lonadinae Oberpr. & Töpfer, subtrib. nov.
Type: Lonas Adans. (Lonas annua (L.) Vines & Druce).
Description — Glabrous annual herbs. Leaves alternate, pinnatisect. Capitula in a dense corymb, discoid. Involucre hemispheric to cylindric. Phyllaries in 3 or 4 rows, with narrow, pale scarious margins. Receptacle narrowly conic, paleate; paleae narrowly obovate, flat to slightly canaliculate, with a central resin canal. Florets hermaphrodite, fertile; corolla 5-lobed, yellow. Achenes narrowly obovoid, round in cross-section or slightly dorsiventrally flattened, with 1 adaxial and 2 lateral ribs; apex with a scarious corona; pericarp with myxogenic cells abaxially and on ribs and with a resin sac apically in adaxial rib. Embryo sac development monosporic. Base chromosome number x = 9.
Distribution — NW Africa, Sicily.
Members — Lonas Adans. (1).
Notes — The unispecific genus Lonas was assigned to the extremely polyphyletic subtribe Matricariinae sensu Bremer & Humphries (1993), who acknowledged that the position of the genus “is difficult to assess” (l.c.: 155). The species L. annua was described by Linnaeus (1753) as a member of the genus Santolina and a close relationship with Santolina and other members of the Santolininae is reasonable both on morphological (receptacular paleae with a central resin duct) and molecular phylogenetic grounds. However, none of the gene and species trees presented here revealed a strongly supported position within the Santolininae; conversely, in the concatenated sequence analysis (Fig. 3), it is strongly supported as a sister-group to a monophyletic Santolininae+Glebionidinae lineage.
16. Lepidophorinae Oberpr. & Töpfer, subtrib. nov.
Type: Lepidophorum Neck. ex Cass. (Lepidophorum repandum (L.) DC.).
Description — Annual, glabrous herbs. Leaves alternate, serrate. Capitula solitary, pedunculate, radiate. Involucre meniscoid to hemispheric. Phyllaries in 3 or 4 rows, with narrow, brown scarious margins. Receptacle convex, paleate; paleae flat to canaliculate, narrowly elliptic to obovate, with a central resin duct. Ray florets female or neuter, sterile; limb yellow. Disc florets hermaphrodite, fertile; corolla 5-lobed, yellow. Achenes of ray florets flat; apex with c. 4 free or basally connate scales. Achenes of disc florets narrowly obovoid, 5-ribbed; apex marginally rounded; pericarp with myxogenic cells along ribs, without resin sacs. Embryo sac development monosporic. Base chromosome number x = 9.
Distribution — SW Europe.
Members — Lepidophorum Neck. ex Cass. (1).
Notes — As in the previous case of Lonas, the annual, unispecific genus Lepidophorum was considered “difficult to place” on morphological and anatomical grounds by Bremer & Humphries (1993: 139), who classified it in their highly polyphyletic subtribe Leucantheminae, which contained also genera presently arranged in subtribes Artemisiinae (Leucanthemella, Nipponanthemum), Glebionidinae (Nivellea) and Leucanthemopsidinae (Hymenostemma, Leucanthemopsis, Phalacrocarpum, Prolongoa). Based on the possession of receptacular paleae with a central resin duct, the genus shows some morphological affinity to Lonadinae and Santolininae. However, both gene trees of the present study (Fig. 1, 2) do not support either affinity, while the genus is unfortunately missing in the species-tree reconstructions due to missing sequence information from the other nuclear markers.
17. Leucantheminae K. Bremer & Humphries in Bull. Nat. Hist. Mus. London, Bot. 23: 136. 1993. – Type: Leucanthemum Mill. (Leucanthemum vulgare Lam.).
Description — Annual or perennial herbs, rarely subshrubs (Leucanthemum, Plagius, Rhodanthemum). Indumentum absent or of basifixed hairs, rarely of medifixed hairs (Rhodanthemum). Leaves alternate or basally opposite, entire, serrate-dentate, lobed or up to 3-pinnatisect. Capitula solitary or in a lax corymb, discoid or radiate. Involucre meniscoid to hemispheric. Phyllaries in 3–5 rows, with narrow to broad scarious margins. Receptacle hemispheric to conic, epaleate. Ray florets female or sterile; limb white, yellow or red (Rhodanthemum). Disc florets hermaphrodite; corolla (4 or)5-lobed, basally often saccate and clasping top of achene; anthers with non-polarized endothecial tissue and a balusterform filament collar. Achenes of ray florets ellipsoid, circular in cross-section, with 5–10 ribs, sometimes dorsiventrally flattened, with 3 adaxial ribs and lateral wings (Daveaua). Achenes of disc florets ellipsoid, circular in cross-section, with 5–10 ribs, rarely dorsiventrally flattened and with 1 abaxial, 2 lateral and 1–3 adaxial ribs (Otospermum); apex marginally rounded or with a scarious and adaxially longer corona, sometimes (Heteromera) with a short and basally callose corona or with 5–9 obovate scales; pericarp with myxogenic cells along ribs and with resin canals between ribs, sometimes (Daveaua, Heteromera) with 3–5 resin sacs apically in ribs, rarely (Otospermum) without any resin ducts. Embryo sac development monosporic. Base chromosome number x = 9.
Distribution — Mediterranean region, Macaronesia, Europe, Asia.
Members — Chlamydophora Ehrenb. ex Less. (1), Chrysanthoglossum B. H. Wilcox & al. (2), Coleostephus Cass. (3), Daveaua Mariz (1), Glossopappus Kunze (1), Heteromera Pomel (2), Leucanthemum Mill. (43), Mauranthemum Vogt & Oberprieler (4), Otospermum Willk. (1), Plagius L'Hèr. ex DC. (3), Rhodanthemum B. H. Wilcox & al. (14).
Notes — Dating back to analyses of nrDNA ITS sequence variation in Oberprieler (2004b), the inclusion of Daveaua, Heteromera and Otospermum into subtribe Leucantheminae has been evident but was never formalized thereafter (Oberprieler & al. 2007, 2009). This was mainly due to the distinctness of the achene-anatomically well-circumscribed generic assemblage around the core genus Leucanthemum with its apomorphic character state of achenes with resin canals and vascular bundles between the ribs, which is lacking in the three mentioned genera. Here, achenes are 5-ribbed and ribs contain vascular bundles, while Daveaua and Heteromera also share the possession of resin ducts in the apical portions of ribs and of dorsiventrally flattened achenes of ray florets (Giroux 1930; Oberprieler 2004b). With the inclusion of Daveaua, Heteromera and Otospermum in the Leucantheminae, as suggested again by our phylogenetic analyses based on the now more comprehensive dataset, the morphological circumscription of the subtribe becomes more heterogeneous; however, it avoids the erecting of uninformative, unigeneric subtribal units where there is a clear evolutionary pattern.
18. Santolininae Willk. in Willkomm & Lange, Prodr. Fl. Hispan. 2: 76. 1870. – Type: Santolina L. (Santolina chamaecyparissus L.).
Description — Shrubs, subshrubs, perennial or annual herbs. Indumentum of basifixed, medifixed or stellate hairs. Leaves alternate, entire, lobed or dentate to 2- or 3-pinnatisect, sometimes vermiform. Capitula solitary or in lax corymbs, radiate, disciform or discoid. Involucre hemispheric or obconic to urceolate (Rhetinolepis), sometimes umbonate (Mecomischus, Santolina). Phyllaries in 3 rows, with narrow to broad scarious margins. Receptacle hemispheric to conic, paleate; paleae flat to canaliculate, often with a central resin duct. Ray florets female or neuter; limb white, orange or yellow. Disc florets hermaphrodite; corolla 5-lobed, basally often saccate and clasping top of achene; anthers with non-polarized endothecial tissue and a balusterform filament collar. Achenes obovoid, circular in cross-section, with 3 flimsy ridges (in Santolina 3–5-angled or slightly dorsiventrally flattened); apex marginally rounded; pericarp consisting of large myxogenic cells in longitudinal rows, without resin sacs (in Santolina sometimes without myxogenic cells). Embryo sac development monosporic (only known in Chamaemelum and Cladanthus). Base chromosome number x = 9.
Distribution — W and S Europe, N Africa, SW Asia.
Members — Chamaemelum Mill. (2), Cladanthus Cass. (5), Mecomischus Coss. ex Benth. & Hook. f. (2), Rhetinolepis Coss. (1), Santolina L. (13).
Notes — The circumscription of Santolininae of Oberprieler & al. (2007) is well-supported both in the cpDNA (Fig. 1) and nrDNA ITS gene trees (Fig. 2), as well as (for a reduced generic sample comprising Chamaemelum, Cladanthus and Rhetinolepis) in the species-tree reconstructions (Fig. 3, 4).
19. Glebionidinae Oberpr. & Vogt in Willdenowia 37: 106. 2007. – Type: Glebionis Cass. (Pyrethrum indicum Roxb. ex Sims. [= Glebionis coronaria (L.) Cass. ex Spach]).
Description — Subshrubs (Argyranthemum) or annual herbs. Indumentum absent or of basifixed hairs (in Heteranthemis with glandular hairs). Leaves alternate, serrate-dentate to 2-pinnatisect. Capitula solitary or in lax corymbs, radiate, rarely (Otoglyphis) discoid or disciform. Involucre meniscoid to hemispheric. Phyllaries in 3–5 rows, with broad scarious margins. Receptacle convex to conic, epaleate. Ray florets female; limb white or yellow. Disc florets hermaphrodite; corolla 5-lobed, rarely (Otoglyphis) lobes with a central resin sac; anthers with non-polarized endothecial tissue and a balusterform filament collar. Achenes of ray florets triquetrous and 2- or 3-winged; achenes of disc florets laterally compressed and 1- or 2-winged, sometimes terete and 10-ribbed; apex marginally rounded or with a corona; pericarp without myxogenic cells or resin sacs, rarely (Nivellea) with myxogenic cells along ribs; in Otoglyphis, circular to only slightly flattened in cross-section, apex marginally rounded or with an adaxial auricle, pericarp with myxogenic cells and sometimes with 2 lateral resin canals; in Endopappus, dorsiventrally flattened, 3-angled with 1 adaxial and 2 lateral ribs; apex with a corona; pericarp with myxogenic cells abaxially and along ribs, without resin sacs. Embryo sac development monosporic, bisporic (Argyranthemum) or tetrasporic (Heteranthemis). Base chromosome number x = 9.
Distribution — Macaronesia, Europe, N Africa, SW Asia.
Members — Argyranthemum Webb (24), Endopappus Sch. Bip. (1), Glebionis Cass. (2), Heteranthemis Schott (1), Ismelia Cass. (1), Nivellea B. H. Wilcox & al. (1), Otoglyphis Pomel (2) [incl. Aaronsohnia Warb. & Eig (1)].
Notes — In its previous circumscription, the subtribe Glebionidinae comprised the four genera Argyranthemum, Glebionis, Heteranthemis and Ismelia and formed a well-supported monophyletic and morphologically well-characterized generic assemblage due to the occurrence of distinctly heteromorphic achenes (achenes of ray florets triquetrous, those of the disc florets terete or laterally flattened). Our present phylogenetic analyses, especially the gene tree based on cpDNA sequence variation (Fig. 1) and the total-evidence tree based on concatenated markers (Fig. 3), indicate that three annual genera [Endopappus, Nivellea and Otoglyphis (the former Aaronsohnia)] are closely related with this core group. In order to keep the number of subtribes in the Anthemideae at a reasonable level, we suggest inclusion of these three genera into the Glebionidinae, which then becomes inevitably more heterogeneous and less characteristic in its circumscription.
The close relationship between the SW Asian species Aaronsohnia factorovskyi Warb. & Eig and the N African Chlamydophora pubescens (Desf.) Coss. & Durieu (based on Cotula pubescens Desf.) led Bremer & Humphries (1993) to transfer the latter taxon to Aaronsohnia. However, by doing so, the two authors did not realize that there is an older generic name available for Cotula pubescens. It was discovered by A. Dobignard (in Dobignard & Chatelain (2011) that Pomel (1874) had described the genus Otoglyphis based on Chlamydophora pubescens and he consequently transferred the subspecies Aaronsohnia pubescens subsp. maroccana (Ball) Fennane & Ibn Tattou to Otoglyphis as an independent species (O. maroccana (Ball) Dobignard). If Aaronsohnia is considered as being congeneric with Otoglyphis following the reasoning of Bremer & Humphries (1993), the latter has priority over the former. Owing to the observation of very similar nrDNA ITS1 sequences of Aaronsohnia factorovskyi and Otoglyphis pubescens (Desf.) Pomel (Gemeinholzer & al. 2006) and the treatment of Matricaria maroccana Ball (≡ Aaronsohnia pubescens subsp. maroccana) as a subspecies of O. pubescens, we propose the following two new combinations:
Otoglyphis factorovskyi (Warb. & Eig) Oberpr. & Vogt, comb. nov. ≡ Aaronsohnia factorovskyi Warb. & Eig in Leafl. Agric. Exp. Sta. Zionist Organ. Inst. 6: 40. 1927.
Otoglyphis pubescens subsp. maroccana (Ball) Oberpr. & Vogt, comb. nov. ≡ Matricaria maroccana Ball in J. Bot. 11: 367. 1873 ≡ Aaronsohnia pubescens subsp. maroccana (Ball) Fennane & Ibn Tattou in Bocconea 8: 18. 1998 ≡ Otoglyphis maroccana (Ball) Dobignard, Index Syn. Fl. Afrique N. 2: 333. 2011.
Author contributions
Christoph Oberprieler and Robert Vogt initiated and conveyed the present study and discussed its results and its nomenclatural consequences. Miriam Stock contributed nrDNA ITS, ETS and cpDNA sequences in the course of a post-doctoral engagement with the Evolutionary and Systematic Botany Group at Regensburg University. Alisha Töpfer completed the dataset during her Master thesis in 2021, while Marco Dorfner helped with phylogenetic reconstructions. Christoph Oberprieler wrote the manuscript and Alisha Töpfer drew the phylogenetic trees.
Acknowledgements
We would like to thank Sabine Härtl and Anja Heuschneider for their technical help in the molecular laboratory of the Evolutionary and Systematic Botany Group at Regensburg University. Agnes Scheunert kindly provided sequence and primer information for the newly established nuclear single- or low-copy markers. Anthony Magee, Inés Álvarez and two anonymous reviewers are thankfully acknowledged for their helpful comments on the manuscript. Additionally, Nicholas Turland is thanked for his great help with handling this contribution and improving it considerably.
References
Appendices
Appendix 1.
List of taxa and sources of plant material used for the current molecular study. When two accession numbers are given under ITS, these represent the ITS1 and ITS2 regions, respectively. Boldface denotes sequences new to science.
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Supplemental content online
See https://doi.org/10.3372/wi.52.52108
Online Fig. S1 (wi.52.52108_OnlineFig_S1.pdf). Phylogeny (gene tree) of Compositae–Anthemideae based on nDNA DSP sequences with subtribal assignment according to Oberprieler & al. (2007, 2019), Sonboli & Oberprieler (2010) and Sonboli & al. (2012). Clade support values (posterior probabilities > 0.9) are indicated.
Online Fig. S2 (wi.52.52108_OnlineFig_S2.pdf). Phylogeny (gene tree) of Compositae–Anthemideae based on nDNA VIP5 sequences with subtribal assignment according to Oberprieler & al. (2007, 2019), Sonboli & Oberprieler (2010) and Sonboli & al. (2012). Clade support values (posterior probabilities > 0.9) are indicated.
Online Fig. S3 (wi.52.52108_OnlineFig_S3.pdf). Phylogeny (gene tree) of Compositae–Anthemideae based on nDNA NPF3.1 sequences with subtribal assignment according to Oberprieler & al. (2007, 2019), Sonboli & Oberprieler (2010) and Sonboli & al. (2012). Clade support values (posterior probabilities > 0.9) are indicated.
Online Resource S1 (wi.52.52108_OnlineResource_S1.nex). Alignment of the plastid gene ndhF and the intergenic spacer region trnL-trnF, including gap-coding information.
Online Resource S2 (wi.52.52108_OnlineResource_S2.nex). Alignment of the nuclear ribosomal repeat (nrDNA ITS), without gap-coding information.
Online Resource S3 (wi.52.52108_OnlineResource_S3.nex). Alignment of the single-copy nuclear marker DSP, including gap-coding information.
Online Resource S4 (wi.52.52108_OnlineResource_S4.nex). Alignment of the single-copy nuclear marker VIP5, without gap-coding information.
Online Resource S5 (wi.52.52108_OnlineResource_S5.nex). Alignment of the single-copy nuclear marker NPF3.1, without gap-coding information.
Online Resource S6 (wi.52.52108_OnlineResource_S6.nex). Concatenated alignment of the total dataset, comprising markers DSP, VIP5, NPF3.1, ITS+ETS, ndhF and trnL-trnF, without gap-coding information.
