The Astereae subtribe Madagasterinae (Asteraceae) sensu Nesom encompassing four Malagasy genera (Apodocephala, Madagaster, Rochonia and Vernoniopsis) is polyphyletic, as Apodocephala is a member of the Malagasy subtribe Lowryanthinae of the tribe Athroismeae. While Madagaster was shown to belong to Astereae, the phylogenetic positions of Rochonia and Vernoniopsis (now Jalantzia) in this tribe remained to be tested with molecular data. Lowryanthinae presently contains Apodocephala with nine species and the monospecific Lowryanthus. The monophyly of Apodocephala remained to be assessed using a comprehensive sampling. The aims were to: (1) assess the phylogenetic placements of Rochonia and Jalantzia (Vernoniopsis) and test the monophyly of Jalantzia; (2) assess phylogenetic relationships within Lowryanthinae; and (3) re-assess the subtribal and generic limits within the tribe Athroismeae. New phylogenetic analyses based on plastid sequence data confirmed the position of Rochonia in Astereae. Jalantzia (Vernoniopsis) was resolved as sister to the subtribe Lowryanthinae and therefore transferred to Athroismeae. A new subtribe, Jalantziinae, is described to accommodate Jalantzia. Apodocephala is paraphyletic with respect to Lowryanthus, which is formally merged with Apodocephala. A description of the emended subtribe Madagasterinae containing Madagaster and Rochonia is presented.
Citation: Bengtson A. & Razafimandimbison S. G. 2024: New subtribal and generic limits in the tribe Athroismeae (Asteraceae) and further disintegration of the subtribe Madagasterinae of the tribe Astereae. – Willdenowia 54: 103–116.
Version of record first published online on 25 April 2024 ahead of inclusion in April 2024 issue.
Introduction
Madagascar is known for its biodiversity and high level of endemism. The daisy family, Asteraceae, with c. 555 species on Madagascar, 86.9 % of which are endemic, is one of the most species-rich flowering plant families (Madagascar Catalogue 2022). The species represent 103 different genera, but only 20 of these are endemic to Madagascar. Five of the endemic genera are formally grouped in two subtribes: the Athroismeae subtribe Lowryanthinae (Bengtson & al. 2017, 2021) and the Astereae subtribe Madagasterinae (Nesom 2020).
Athroismeae, as defined by Bengtson & al. (2017), is a small, morphologically diverse tribe, whose circumscription has gradually changed over the years (Panero & Funk 2002; Wagstaff & Breitwieser 2002; Panero 2005; Anderberg 2009; Pruski 2014; Bengtson & al. 2017, 2021). Bengtson & al. (2017) presented the first molecular phylogenetic study of the tribe, which resulted in an amended circumscription. The tribe currently consists of ten genera classified in four morphologically diverse subtribes (Anisopappinae, Athroisminae, Lowryanthinae and Symphyllocarpinae; Bengtson & al. 2017, 2021). Lowryanthinae consist of two genera: Lowryanthus Pruski and Apodocephala Baker. Lowryanthus was described by Pruski (2014), who postulated it to be closely related to the Blepharispermum group (= subtribe Athroisminae). Bengtson & al. (2017) later confirmed its position in the tribe Athroismeae, where it was resolved as sister to subtribe Athroisminae. Lowryanthus was, however, placed in its own subtribe, Lowryanthinae, mainly due to differences in synflorescences and capitula. Lowryanthus is a monospecific genus endemic to Madagascar and consists of shrubs or small trees with red synflorescences with coral-red discoid capitula and florets with reddish to pink corollas (Fig. 1B). A recent phylogenetic study by Bengtson & al. (2021) revealed the Malagasy endemic genus Apodocephala to be sister to Lowryanthus and therefore another member of subtribe Lowryanthinae. This study, however, included only two of the nine described Apodocephala species. The Apodocephala species most morphologically resembling Lowryanthus were not included and, therefore, the phylogenetic relationships within subtribe Lowryanthinae remained unclear.
Fig. 1.
A: Apodocephala pauciflora; B: Lowryanthus rubens; C: Jalantzia (Vernoniopsis) caudata; D: Rochonia cinerarioides; E: Madagaster sp. – Photographs by S. E. Rakotoarisoa (A; CC BY-NC © 2023), M. Thulin (B; CC BY-NC-SA © 2023), S. Razafimandimbison (C, E) and M. Arnerup (D).
Apodocephala was earlier placed in the tribe Astereae, where it has, based on morphology, been associated with the Malagasy genera Vernoniopsis Humbert, Rochonia DC. and Madagaster G. L. Nesom (Humbert 1960; Bremer 1994; Nesom 2020; Fig. 1A, C, D, E), later classified in Nesom's (2020) subtribe Madagasterinae. Apodocephala was, however, omitted from Astereae by Nesom & Robinson (2007) in their account of the tribe. Subtribe Madagasterinae are characterized by their arborescent habit, coriaceous and abaxially tomentose leaves and their caudate anthers. Bengtson & al. (2021) have shown Madagasterinae to be non-monophyletic, because Apodocephala belongs to the tribe Athroismeae. Apodocephala consists of nine species of shrubs or trees with discoid capitula and florets with white or whitish corollas (Fig. 1A). Molecular phylogenetic studies have confirmed the position of Madagaster within Astereae (Brouillet & al. 2009), but the phylogenetic placement of the Malagasy Rochonia and Vernoniopsis within Astereae and their relationships to Apodocephala remain untested by molecular analysis. Rochonia encompasses four species and has campanulate, radiate capitula with yellow ray florets (Fig. 1D). This genus is morphologically more similar to Madagaster. Vernoniopsis, however, resembles Apodocephala in having discoid 1- to few-flowered capitula with cylindric involucres and florets with whitish corollas. Vernoniopsis was originally described as monospecific with two subspecies differing in leaf and cypsela sizes (Humbert 1955), V. caudata (Drake) Humbert subsp. caudata and subsp. lokohensis Humbert. The latter subspecies was later raised to species level (Callmander & Phillipson 2011). The monophyly of Vernoniopsis has never been tested.
The aims of the study were to: (1) assess the phylogenetic placements of Rochonia and Vernoniopsis and test the monophyly of Vernoniopsis as defined by Callmander & Phillipson; (2) assess phylogenetic relationships within the subtribe Lowryanthinae; and (3) to re-assess the subtribal and generic limits within the tribe Athroismeae.
Material and methods
Taxon sampling
Herbarium specimens from MO, P and S (herbarium codes according to Thiers 2023+), as well as newly collected specimens from Madagascar were included in the study. Thirteen specimens of Apodocephala, representing all but one species (no specimens of A. coursii Humbert suitable for DNA-extraction could be located), both species of Vernoniopsis, and Rochonia cinerarioides DC. were included in the molecular study. The systematic positions of Vernoniopsis and Rochonia were analysed in a large dataset, including 139 taxa and representing a wide coverage of Asteraceae tribes. Molecular phylogenetic analyses of the Athroismeae, with a focus on the subtribe Lowryanthinae were then conducted, including 60 taxa and representatives of all known genera of the tribe. Four different loci were sequenced for the study, two from the nuclear genome (ETS, ITS) and two from the plastid genome (ndhF, trnL-trnF). A complete list of sampled taxa and voucher information is given in Appendix 1.
DNA extraction, amplification and sequencing
DNA was extracted from herbarium material or, if available, from silica-gel dried leaves, using a DNeasy Plant Mini Kit (Qiagen, Hilden, Germany) according to the manufacturer's instructions. The DNA regions of interest were amplified using Hot Start Mix RTG beads (GE Healthcare, Little Chalfont, United Kingdom) following the manufacturer's standard protocol. The nuclear ribosomal (nr) DNA external transcribed spacer (ETS) was amplified using primers Ast-1 (Markos & Baldwin 2001) and 18S-ETS (Baldwin & Markos 1998), and the nrDNA internal transcribed spacer (ITS, including ITS1, ITS2 and the 5.8S gene) was amplified using primers 5.8SRPEny (Nylinder & al. 2013), 5.8F-chrys (Howis & al. 2009), 18SF and 26SR (Rydin & al. 2004). The plastid DNA ndhF gene was amplified using primers RJ1, RJ14 (Kim & Jansen 1995), ndhF16 (Källersjö & al. 2000), ndhF5 (Olmstead & Sweere 1994), 1750R-Ast2, 1650F-Ast (Nylinder & al. 2013), ndhF431F (Eldenäs & al. 1999) and ndhF520R-Ast (Anderberg & Swenson 2003), and the plastid trnL-trnF region (including the trnL in-tron and trnL-trnF intergenic spacer) with the “c”, “d”, “e” and “f” primers of Taberlet & al. (1991). All regions were amplified following the thermal profile described in Bengtson & Anderberg (2018). Amplified products were purified using one portion of Exonuclease I (20u/µl) and four portions of FastAP Thermosensitive Alkaline Phosphatase (1u/µl) (Thermo Scientific; Vilnius, Lithuania). Purified PCR-products were sequenced by Macrogen Europe (Amsterdam, Netherlands, https://www.macrogen-europe.com/). Resulting sequences were assembled and carefully checked and edited using the Staden package (Staden 1996). New sequences have been submitted to GenBank, and accession numbers are cited in the voucher list (Appendix 1).
Phylogenetic analyses
Sequences were aligned using MUSCLE v.3.8.425 (Edgar 2004) as implemented in AliView v.1.24 (Larsson 2014) and manually edited using BioEdit v.7.2.5 (Hall 1999). Two different datasets were compiled and analysed ( Supplementary appendices S1 (wi.54.54107_Supplementary_appendix_S1_ndhF_matrix.nex), S2 (wi.54.54107_Supplementary_appendix_S2_combined_matrix.nex)); we initially performed analyses of an ndhF matrix, including 139 accessions and a representing wide coverage of the Asteraceae tribes, in order to determine the tribal positions of Vernoniopsis and Rochonia within the family. A second dataset with a focus on the tribe Athroismeae consisting of ETS, ITS, ndhF and trnL-trnF sequence data from 60 accessions was then analysed. Boopis anthemoides Juss. (Calyceraceae) was used as outgroup in analyses of the Asteraceae ndhF matrix and Callilepis salicifolia Oliv. in analyses of the combined Athroismeae dataset, following Bengtson & al. (2017). All the analyses were conducted with Bayesian and parsimony methods. Prior to analyses of the combined dataset each region was analysed separately to check for incongruences by simply comparing the topologies.
Bayesian inference analyses were conducted using MrBayes v.3.2.2 (Ronquist & al. 2012) using the online XSEDE platform in the CIPRES Science Gateway (Miller & al. 2010). Nucleotide substitution models were set to GTR+I+G for the Asteraceae ndhF dataset, and to GTR+G for ETS and GTR+I+G for ITS and the plastid markers (ndhF, trnL-trnF) for the combined dataset, selected as best fit for the data using the Akaike information criterion (AIC) as implemented in jModeltest v. 2.1.10 (Guindon & Gascuel 2003; Darriba & al. 2012). Analyses consisted of two independent runs, with eight chains each. The Markov Chain Monte Carlo (MCMC) was run for 75 million generations with a sampling frequency of 7500 for the ndhF matrix, and for 50 million generations with a sampling frequency of 5000 for the combined dataset. Convergence of Markov chains was examined using Tracer v.1.7.1 (Rambaut & al. 2018) as well as by checking the average standard deviation values of split frequencies. The first 25 % of the trees were excluded as a burn-in phase. Consensus trees were visualized using FigTree v.1.4.4 ( http://tree.bio.ed.ac.uk/software/figtree/). Maximum parsimony analyses were conducted using PAUP v.4.0a (Swofford 2002), using the settings described in Bengtson & al. (2021). All analyses were run multiple times using the settings described above.
Results
The Asteraceae ndhF dataset consisted of 2292 aligned characters, 559 of which were parsimony informative, and the combined Athroismeae dataset of 4436 aligned characters, 773 of which were parsimony informative. The parsimony analysis of the ndhF dataset yielded 6840 most parsimonious trees, 2912 steps long (consistency index, CI = 0.38; retention index, RI = 0.68, excluding uninformative characters), and the parsimony analysis of the Athroismeae dataset yielded two most parsimonious trees, 2717 steps long (CI = 0.51, RI = 0.83). Analyses of separate regions resulted in less resolved trees. One incongruence was detected in Bayesian analyses of the ITS region where Anisochaeta DC. was resolved as sister to Vernoniopsis (posterior probability, PP = 0.93, not shown).
Bayesian and parsimony analyses produced trees with similar overall topologies. A majority-rule consensus tree from a Bayesian analysis of the ndhF dataset, including representatives from the entire Asteraceae, is shown in Fig. 2. The analyses resolved Rochonia cinerarioides as part of a clade consisting of members of the tribe Astereae (posterior probability, PP = 1.0, bootstrap support, BS = 100, Fig. 2). The Vernoniopsis specimens were resolved as monophyletic (PP = 1.0, BS = 100) and placed as sister to the Lowryanthinae subtribe (PP = 0.99, BS = 59, Fig. 2) within a poorly supported tribe Athroismeae (PP = 0.85, BS < 50, Fig. 2). A majority-rule consensus tree from a Bayesian analysis of the Athroismeae dataset, consisting of both nuclear (ETS, ITS) and plastid (ndhF, trnL-trnF) data is presented in Fig. 3. The analysis confirmed the position of Vernoniopsis within Athroismeae (PP = 1.0, BS = 87) where it was resolved as sister to the subtribe Lowryanthinae (PP = 0.97, BS < 50, Fig. 3). The subtribe Lowryanthinae, consisting of Apodocephala and Lowryanthus, was resolved as monophyletic with high support (PP = 1.0, BS = 100). The analysis resolved L. rubens within Apodocephala, in a poorly supported clade together with A. radula Humbert and A. minor Scott Elliot (PP = 0.75, BS = 61, Fig. 3). The remaining Apodocephala species were resolved in a well-supported clade (PP = 1.0, BS = 100, Fig. 3). Apodocephala urschiana Humbert, A. angustifolia Humbert, A. begueana Humbert, A. pauciflora Baker var. pauciflora and one undetermined Apodocephala formed a well-supported subclade (PP = 1.0, BS = 85), and A. multiflora Humbert, A. oliganthoides Humbert and A. pauciflora var. cacuminum Humbert formed another highly supported subclade (PP = 0.98, BS = 75, Fig. 3).
Discussion
Phylogenetic positions of Vernoniopsis and Rochonia
Nesom (2020) placed the Malagasy genera Apodocephala, Vernoniopsis, Rochonia and Madagaster in his new subtribe, Madagasterinae of the tribe Astereae, based on their arborescent habit with coriaceous abaxially tomentose leaves, caudate anther thecae and isolated geographic distribution. Madagaster has been confirmed to be a member of the tribe Astereae (Brouillet & al. 2009); however, Apodocephala was recently shown to belong to the tribe Athroismeae and transferred there (Bengtson & al. 2021), implying the non-monophyly of Madagasterinae as defined by Nesom (2020). The monophyly of Madagasterinae is further rejected by our analyses, because Vernoniopsis was resolved sister to the Apodocephala-Lowryanthus clade (Fig. 2, 3). Vernoniopsis is therefore another addition to the Athroismeae (Fig. 2, 3).
The phylogenetic position of Rochonia (here represented by R. cinerarioides) within Astereae is strongly supported (Fig. 2), consistent with Nesom (2020). Rochonia consists of four species of shrubs or subshrubs with radiate capitula bearing ray florets with yellow corollas (Fig. 1D). The genus resembles Madagaster in morphology, and Humbert (1932) even described the taxa currently placed under Madagaster and Rochonia (then Aster L.) as mainly differing in the colour of the ray floret corollas (Madagaster have ray florets with white to bluish corollas). Nesom (1993) described the genus Madagaster for the white-rayed species, considered to be a lineage separate from, but close to, Rochonia. We agree that Madagaster and Rochonia are likely to be closely related based on their morphological similarities; however, whether they are sisters remains to be seen. In summary, only two out of the four genera of Nesom's (2020) subtribe Madagasterinae, Madagaster and Rochonia, remain.
Monophyly of Vernoniopsis (now Jalantzia)
Our analyses strongly support the monophyly of Vernoniopsis (here represented by its two species, V. caudata (Drake) Humbert and V. lokohensis (Humbert) Callm. & Phillipson; Callmander & Phillipson 2011) and its phylogenetic position in the tribe Athroismeae as delimited by Bengtson & al. (2021), where it is resolved as sister to the Apodocephala-Lowryanthus clade (Fig. 2, 3). This finding is inconsistent with Bremer (1994) and Nesom (2020), who classified the genus in the tribe Astereae. Members of Vernoniopsis are shrubs or small trees with coriaceous leaves and discoid homogamous capitula containing 1–4 florets with white corollas (Fig. 1C; Humbert 1960; Callmander & Phillipson 2011). Vernoniopsis caudata, the generitype, was originally described by Drake (1899) as Vernonia caudata Drake because of its Vernonia-like habit and inflorescences, inconsistent with our results. Humbert (1955) totally rejected this taxonomic decision and described his new genus Vernoniopsis to accommodate Vernonia caudata in the tribe Astereae based on differences in the stigmatic surfaces of the style branches. The name Vernoniopsis was recently noted to be an illegitimate later homonym of Vernoniopsis Dusén and has therefore been replaced by Jalantzia D. J. N. Hind (Hind & Langhorne 2024). The recognition of Vernoniopsis (now Jalantzia) at generic level is consistent with our findings. Jalantzia (Vernoniopsis) has been suggested to be closely related to the Malagasy genus Apodocephala based on their discoid capitula with white corollas and the presence of shortly caudate anthers (Humbert 1960; Bremer 1994; Nesom 2020). The molecular phylogenetic analyses here confirm the close relationship of Apodocephala and Jalantzia (Fig. 2, 3). Jalantzia differs from Apodocephala in having epaleate receptacles and a pappus of scabrid bristles, whereas Apodocephala has paleate receptacles and lacks a true pappus. Therefore, we maintain the current generic status of Jalantzia.
Fig. 2.
Bayesian fifty-percent majority-rule consensus tree from an analysis of the Asteraceae ndhF dataset, showing position of Rochonia within Astereae and Jalantzia (Vernoniopsis) within Athroismeae. Numbers above branches indicate posterior probability (PP) and bootstrap values (BS), bootstrap values <50 are indicated by a dash. Scale bar shows number of substitutions per site.
Fig. 3.
Bayesian fifty-percent majority-rule consensus tree from an analysis of the combined Athroismeae dataset (including ETS, ITS, ndhF and trnL-trnF). Numbers above branches indicate posterior probability (PP) and bootstrap values (BS), bootstrap values <50 are indicated by a dash. Scale bar shows number of substitutions per site.
Table 1.
Distinguishing characters between Apodocephala pauciflora var. pauciflora and A. pauciflora var. cacuminum.
Further, our analyses support the recognition of Vernoniopsis caudata subsp. lokohensis Humbert at species level (Callmander & Phillipson 2011). Jalantzia (Vernoniopsis) caudata (Drake) D. J. N. Hind and J. lokohensis (Humbert) D. J. N. Hind do not grow sympatrically. The former commonly grows along the littoral forests of the eastern coast of Madagascar, while the latter is restricted to the highland rainforests of the Marojejy massif in northeastern Madagascar between 1300 and 2000 m in elevation. In other words, Jalantzia (Vernoniopsis) contains two geographically distinct lineages, the northeastern group (J. lokohensis) and the eastern-southeastern group (J. caudata). A similar pattern has recently been reported by Razafimandimbison & al. (2022) in the Malagasy Schismatoclada farahimpensis Homolle (Rubiaceae), which was resolved in two geographically and morphologically distinct lineages: northern and southern groups, that could be recognized at subspecies level (Razafimandimbison, unpublished data).
Phylogenetic relationships within Apodocephala
Apodocephala currently consists of nine species of trees or shrubs with discoid paleate capitula in terminal corymbiform-paniculate inflorescences, all endemic to Madagascar: A. angustifolia, A. begueana, A. coursii, A. minor, A. multiflora, A. oliganthoides, A. pauciflora, A. radula and A. urschiana. Our analyses demonstrate that Apodocephala is paraphyletic with respect to the monospecific Malagasy genus Lowryanthus (here represented by two individuals of L. rubens). This is inconsistent with Bengtson & al. (2021), who resolved Lowryanthus as sister to two species of Apodocephala (Fig. 3). Apodocephala is resolved into two major clades: one containing A. minor, A. radula and L. rubens and the other formed by A. angustifolia, A. begueana, A. multiflora, A. oliganthoides, A. pauciflora and A. urschiana. Apodocephala and Lowryanthus mainly differ in the colour of the peduncles, capitula and florets (Fig. 1A, B). The latter has a striking appearance with bright red inflorescences and florets, whereas Apodocephala has florets with white or whitish corollas. Aside from that, L. rubens resembles Apodocephala, both consist of shrubs or trees with discoid mainly few-flowered paleate capitula in terminal corymbiform-paniculate inflorescences and have cypselas that lack a true pappus. Bengtson & al. (2021) noted additional similarities in the cypselas of Lowryanthus and Apodocephala (Fig. 4). Lowryanthus has geniculaterostrate cypselas with a tightly curved rostrum (Pruski 2014), a character also found in several species of Apodocephala. The flattened rostrate cypselas of A. coursii and A. radula (see Humbert 1962: 86) especially resemble those of L. rubens, but A. minor and A. urschiana also have cypselas with a narrowed curved rostrum (Fig. 4; Humbert 1960, 1962). The character therefore occurs in both clades (Fig. 3, 4).
The two major clades of Apodocephala are geographically separated. Apodocephala minor and A. radula are both found in close geographical proximity of the known localities of Lowryanthus rubens in southeastern Madagascar. However, the three species do not grow sympatrically and occupy different habitats. Lowryanthus rubens is found in low-elevation humid evergreen forests from 100–300 m in elevation, whereas A. radula is found in siliceous rocky habitats at higher elevations and A. minor grows in rocky habitats at low elevations (Humbert 1960; Pruski 2014). The remaining sampled Apodocephala species form a well-supported clade (Fig. 3) and have a much wider geographic distribution along eastern Madagascar, ranging from Ivohibe in the southeast to Daraina in northern Madagascar. It can be concluded that geographic proximity is sometimes a better predictor of evolutionary history than morphology; a similar pattern has recently been reported from the Malagasy endemic Rubiaceae genera Payera Baill. and Schismatoclada Baker (Razafimandimbison & al. 2022). Despite the geographical separation of the two clades, we argue that Lowryanthus should be formally merged in Apodocephala (which has the priority over the former), because there is no morphological difference between the two clades that would justify dividing Apodocephala in two.
Humbert (1955) divided Apodocephala pauciflora into two varieties, A. pauciflora var. pauciflora and A. pauciflora var. cacuminum, differing in leaf size and shape (see Table 1) as well as in shape of involucral bracts and capitulum size, where A. pauciflora var. cacuminum appears to have somewhat larger capitula. Morphological comparisons also show differences in the shape of the cypselas, which are shorter and more subprismatic in var. cacuminum (Fig. 4G, H). The two varieties differ in distribution and habitat. Apodocephala pauciflora var. pauciflora grows in rainforests at 800–1900 m in elevation and has a wider distribution ranging from Marojejy in the northeast to Fianarantsoa in central Madagascar. In contrast, A. pauciflora var. cacuminum is restricted to the Marojejy massif in the northeast, where it is found in ericoid vegetation in rocky places from 1300 to over 2000 m in elevation (Humbert 1955, 1960). Further, A. pauciflora var. pauciflora and var. cacuminum also appear to differ in flowering time (Table 1). Analyses place the two varieties in different clades, a specimen of A. pauciflora var. pauciflora is placed sister to A. begueana, in a clade also consisting of A. urschiana and A. angustifolia, whereas two specimens of A. pauciflora var. cacuminum form a monophyletic group sister to A. oliganthoides in a clade comprising also A. multiflora (Fig. 3). Apodocephala pauciflora var. cacuminum resembles A. oliganthoides in having oblanceolate leaves and capitula with rounded involucral bracts. Our results support that A. pauciflora var. pauciflora and var. cacuminum should be considered separate species.
Fig. 4.
Cypselas – A, B: Lowryanthus rubens, Razafimandimbison & al. 1531 (S); C, D: Apodocephala radula, Humbert 20708 (S); E: A. minor, Sabouraeu (P); F: A. urschiana, McPherson & van den Werff 16551 (MO); G: A. pauciflora var. pauciflora, Turk & Randriamanatena 203 (MO); H: A. pauciflora var. cacuminum, Razafimandimbison & Razafindrahaja 2951 (S); I: A. oliganthoides, Razafimandimbison & Razafindrahaja 2975 (S); J: A. multiflora, Ranarivelo & Ravelnarivo 771 (MO); K: A. begueana, Service Forestier de Madagascar 13551-SF (P); L: A. angustifolia, Rakotomalala & Narison 124 (MO). – All scale bars = 1 mm.
Apodocephala coursii could not be included in the molecular study, but morphological comparison shows similarities to A. radula and A. rubens, and it is likely to be closely related to those species. Apodocephala coursii, A. radula and A. rubens all have similar flattened cypselas with a curved rostrum, and A. coursii and A. rubens also have cypselas with long marginal and apical trichomes (Humbert 1960, 1962; Pruski 2014). Apodocephala coursii, A. radula and A. rubens all have distributions in southeastern Madagascar. Apodocephala coursii is only known from the Atsimo-Atsinanana region in eastern Madagascar where it grows in rainforest vegetation (Humbert 1962).
Based on the evidence presented above, two new combinations are made: Apodocephala rubens (Pruski) Bengtson & Razafim. and A. cacuminum (Humbert) Bengtson & Razafim. (see below).
Implications on the subtribal classification of the tribe Athroismeae
Athroismeae sensu Bengtson & al. (2021) is currently divided into four morphologically distinct subtribes: Anisopappinae, Athroisminae, Lowryanthinae and Symphyllocarpinae; in addition to this, the tribe also contains the unplaced monospecific Anisochaeta (Bengtson & al. 2017). The subtribe Lowryanthinae is endemic to Madagascar and now encompasses the broadly defined Apodocephala (including Lowryanthus). The subtribe has earlier been placed as sister to subtribe Athroisminae (Bengtson & al. 2017, 2021). Similar obcompressed carbonized asymmetrically rostrate cypselas, and cypselas with long marginal and apical twin hairs, occur in members of both subtribes (Humbert 1960; Eriksson 1990, 1992, 1995; Pruski 2014), and this is also what first led Pruski (2014) to place Lowryanthus in Athroismeae. These characters are, however, not found in Jalantzia (Vernoniopsis). Phylogenetic analyses place Jalantzia here as sister to subtribe Lowryanthinae as defined by Bengtson & al. (2021), and the morphological similarities to Apodocephala support the position of Jalantzia as close to Lowryanthinae. Jalantzia, however, differs from the members of Lowryanthinae in having epaleate receptacles and a true pappus of scabrid bristles, and we have therefore chosen not to include this Malagasy genus in subtribe Lowryanthinae but instead to describe a new subtribe, Jalantziinae, to accommodate Jalantzia.
Taxonomic treatment
Athroismeae
Apodocephala rubens (Pruski) Bengtson & Razafim., comb. nov. ≡ Lowryanthus rubens Pruski in Phytoneuron 2014(51): 1. 2014. – Holotype: Madagascar, Toliara, Anosy Région, Bemangidy Forest, Lowry P. P. II, Rabenantoandro J., Randriatafika F., Lowry E., Ramisy E. & Mara B. 6648. (MO [barcode 2383282 / accession no. 6012800 image!]; isotypes: NY [barcode 02361522 image!], P [barcode P00722630 image!], S [herbarium no. S08-78]!, TAN, US [barcode 01268912 image!]).
Apodocephala cacuminum (Humbert) Bengtson & Razafim., comb. & stat. nov. ≡ Apodocephala pauciflora var. cacuminum Humbert in Mém. Inst. Sci. Madagascar, Sér. B, Biol. Vég. 6: 158. 1955. – Lectotype (designated here): Madagascar, sommet oriental du Massif de Marojejy, 1949, Humbert & Cours 23762 (P [barcode P00435128 image!]; isolectotype: P [barcode P00435129 image!]).
Note — The type specimen in P indicated in the protologue is actually a gathering consisting of two duplicate specimens, with no indication in the protologue, or on the specimens, as to which is the holotype and which is the isotype. A holotype cannot consist of two specimens (Art. 8.1). As a result, a lectotypification is needed.
Jalantziinae Bengtson & Razafim., subtrib. nov.
Type: Jalantzia D. J. N. Hind in Curtis's Bot. Mag. 40: 410. 2024 (≡ Vernoniopsis Humbert in Mém. Inst. Sci. Madagascar, Sér. B, Biol. Vég. 6: 154. 1955, nom. illeg. [non Vernoniopsis Dusén in Beih. Bot. Centralbl., Abt. 2, 38: 284. 1921]).
Description — Shrubs or trees, 1–8 m tall. Leaves oblanceolate, coriaceous, pinnately veined, margin entire. Inflorescence terminal, corymbiform. Capitula discoid, epaleate; florets 1–4; corollas white to whitish. Cypselas oblong, ribbed, glabrous. Pappus of scabrid bristles.
Genus — Jalantzia D. J. N. Hind.
Astereae
Madagasterinae G. L. Nesom in Phytoneuron 2020(53): 28. 2020, emend. Bengtson & Razafim. – Type: Madagaster G. L. Nesom.
Description — Subshrubs, shrubs or small trees. Leaves coriaceous, glabrous or abaxially tomentose, eglandular, venation camptodromous to brochidodromous. Inflorescences terminal and 1-headed to corymboid. Involucres campanulate; receptacles epaleate; ray limbs white to blue or yellow; disc florets bisexual, corolla lobes triangular to linear-lanceolate; anther thecae bases caudate. Cypselas oblong-cylindric to fusiform, subterete, 4–10-veined, eglandular. Pappus of barbel-late bristles.
Genera — Madagaster G. L. Nesom, Rochonia DC.
Conclusions
The Malagasy Rochonia is confirmed to be a member of the tribe Astereae, whereas Vernoniopsis (now Jalantzia) is resolved as sister to the Apodocephala-Lowryanthus clade and therefore another addition to the growing tribe Athroismeae. The non-monophyly of the Astereae subtribe Madagasterinae is further supported. This group now only contains the Malagasy genera Madagaster and Rochonia, and a description of the emended subtribe Madagasterinae is presented. Phylogenetic analyses demonstrate the paraphyly of Apodocephala with respect to the Malagasy monospecific Lowryanthus, and a broad delimitation of Apodocephala (including Lowryanthus) was adopted to render this genus monophyletic. The newly re-circumscribed Apodocephala was resolved in two geographically segregated clades. The Athroismeae now consist of ten genera that are currently classified in five morphologically different subtribes (although Anisochaeta is still unplaced). Much remains unclear regarding how the different subtribes and the Athroismeae as a whole have evolved. Also, the backbone of the tribe is still largely unresolved. It is not unlikely that more additions to the tribe are in the Malagasy flora.
Acknowledgements
The authors would like to thank the Missouri Botanical Garden (MO) and the Muséum National d'Histoire Naturelle (P) herbaria for providing loans. A special thank you to Myriam Gaudeul (P) for sending leaf material of Apodocephala begueana and A. minor for DNA extraction; the DGF (Direction Générale des Forêts) and MNP (Madagascar National Parks) in Madagascar for issuing collecting and exportation permits (permit no. 005/20/ MEDD/SG/DGEF/DGRNE) for SGR in 2020; the Missouri Botanical Garden, Madagascar Program for logistical support; the Parc Botanique et Zoologique de Tsimbazaza and the Missouri Botanical Garden, Madagascar Program (F. Lantoarisoa) for arranging collecting and exportation permits for SGR. We would also like to thank the two anonymous reviewers, whose comments have greatly improved the manuscript; Marcus Arnerup and Jennifer Kearey for help with photos of cypselas; Solofo Eric Rakotoarisoa, Mats Thulin and Marcus Arnerup for allowing us to use their photographs; and Jens Klackenberg for helpful advice on nomenclature. Financial support was received from the Royal Swedish Academy of Sciences (to SGR) and the Harald E. Johanssons fund and Stiftelsen Hierta Retzius fund through the Royal Swedish Academy of Sciences (to AB).
© 2024 The Authors ·
This open-access article is distributed under the CC BY 4.0 licence
References
Appendices
Appendix 1
Voucher information and GenBank accession numbers for sequences used in the phylogenetic study. Taxon, voucher (including country of origin, collector and herbarium), and GenBank accession numbers for ETS, ITS, ndhF and trnL–trnF. Additional Asteraceae ndhF sequences with GenBank accession numbers. A dash (–) indicates missing data. An asterisk (*) indicates sequences generated for this study.
Athroismeae dataset: Anisochaeta mikanioides DC., South Africa, Brand, Abbott & Bosch 478 (S), KY209964, KY210088, KY210128, KY210047; Anisopappus alternifolius (Less.) Bengtson & Anderb., Madagascar, Anderberg & al. 249 (S), KY209939, KY210065, KY210105, KY210023; Anisopappus athanasioides Paiva & S. Ortiz, Angola, da Silva 2070 (S), KY209943, KY210068, KY210108, KY210026; Anisopappusbrandbergensis (P. P. J. Herman) Bengtson & al., Namibia, Nordenstam 2548 (S), KY209971, KY210095, KY210135, KY210054; Anisopappus buchwaldii (O. Hoffm.) Wild, Tanzania, Hedrén & al. 565 (S), HE862088, HE861963, HE862290, HE974615; Anisopappus chinensis Hook. & Arn., Nigeria, Hepper 2894 (S), KY209931, KY210057, KY210098, KY210015; Anisopappus corymbosus Wild, Angola, Kers 3622 (S), KY209968, KY210092, KY210132, KY210051; Anisopappus grangeoides (Vatke & Höpfner ex Klatt) Merxm., Angola, Fritsche 88 (S), KY209932, KY210058, KY210099, KY210016; Anisopappus holstii (O. Hoffm.) Wild, Tanzania, Greenway & Polhill 11667 (S), KY209933, KY210059, KY210100, KY210017; Anisopappus kirkii (Oliv.) Brenan, Zimbabwe, Goldsmith 103/68 (S), KY209934, KY210060, KY210101, KY210018; Anisopappus lastii (O. Hoffm.) Wild, Tanzania, Tanner 409 (S), KY209936, KY210062, KY210102, KY210020; Anisopappus latifolius (S. Moore) B. L. Burtt, South Africa, Codd 8304 (PRE), KY209935, KY210061, AF063068, KY210019; Anisopappus oliveranus Wild, Tanzania, Eriksson & al. 564 (S), HE862089, HE861964, HE862291, HE974616; Anisopappus pinnatifidus (Klatt) O. Hoffm. ex Hutch., Namibia, Nordenstam 2273 (S), KY209938, KY210064, KY210104, KY210022; Anisopappus smutsii Hutch., South Africa, Sidey 3278 (S), KY209940, U84768, AF063070, KY210024; Anisopappus stuhlmannii (O. Hoffm.) Bengtson & al., Tanzania, Thulin & Mhoro 1023b (UPS), KY209972, KY210096, KY210136, KY210055; Apodocephala angustifolia Humbert, Madagascar, Rakotomalala & al. 217 (MO MO04882274), OQ410980*, OQ429281*, OQ427102*, OQ410993*; Apodocephala begueana Humbert, Madagascar, Service Forestier de Madagascar 13551-SF (P P03997213), –, OQ429289*, –, OQ411001*; Apodocephala minor Scott Elliott, Madagascar, Sabouraeu (P P00605013), –, OQ429288*, –, OQ411000*; Apodocephala multiflora Humbert, Madagascar, Miller & Randrianasolo 4657 (MO MO3762392), OQ410978*, OQ429279*, –, OQ410991*; Apodocephala oliganthoides Humbert, Madagascar, Razafimandimbison & al. 2975 (S S20-19252), MZ352988, MZ352991, MZ352997, MZ352994; Apodocephala oliganthoides, Madagascar, Ravelonarivo & al. 2710 (MO MO6335251), OQ410983*, OQ429284*, OQ427105*, OQ410996*; Apodocephala pauciflora var. cacuminum Humbert, Madagascar, Razafimandimbison & al. 2951 (S S20-19242), MZ352987, MZ352990, MZ352996, MZ352993; Apodocephala pauciflora var. cacuminum, Madagascar, Rakotovao & al. 2861 (MO MO6180688), OQ410988*, OQ429291*, OQ427109*, OQ411003*; Apodocephala pauciflora Baker var. pauciflora, Madagascar, Turk & Randriamanatena 203 (MO MO5814955), OQ410987*, OQ429290*, OQ427108*, OQ411002*; Apodocephala radula Humbert, Madagascar, Humbert 20708 (S S-G-549), OQ410976*, OQ429277*, OQ427098*, OQ410989*; Apodocephala sp., Madagascar, Randrianaivo & al. 532 (MO MO5333410), OQ429280*, OQ429280*, OQ427101*, OQ410992*; Apodocephala urschiana Humbert, Madagascar, Randrianasolo & Solo 10 (MO MO5814962), OQ410981*, OQ429282*, OQ427103*, OQ410994*; Apodocephala urschiana, Madagascar, van den Werff & al. 13754 (MO MO5814948), OQ410982*, OQ429283*, OQ427104*, OQ410995*; Artemisiopsis villosa (O. Hoffm.) Schweick., Namibia, Volk 1076 (S), KY209966, KY210090, KY210130, KY210049; Athroisma boranense Cufod., Ethiopia, Eriksson 751 (S), KY209944, KY210069, KY210109, KY210027; Athroisma gracile (Oliv.) Mattf., Kenya, Eriksson & al. 612 (S), KY209945, KY210070, KY210110, KY210028; Athroisma hastifolium Mattf., Tanzania, Eriksson & al. 535 (S), KY209946, AF229258, KY210111, KY210029; Athroisma inevitabile T. Erikss., Uganda, Chandler 866 (S), KY209947, KY210071, KY210112, KY210030; Athroisma laciniatum DC., India, Helfer 189 (S), KY209948, KY210072, KY210113, KY210031; Athroisma pinnatifidum T. Erikss., Madagascar, Eriksson & al. T954 (S), KY209949, KY210073, KY210114, KY210032; Athroisma stuhlmannii O. Hoffm., Tanzania, Eriksson & al. 539 (S), KY209950, KY210074, KY210115, KY210033; Blepharispermum arcuatum T. Erikss., Tanzania, Eriksson & al. 561 (S), KY209953, KY210077, KY210118, KY210036; Blepharispermum hirtum Oliv., Oman, Kilian & Hein NK 5375 (S), KY209954, KY210078, KY210119, KY210037; Blepharispermum pubescens S. Moore, Uganda, Taylor 1682 (S), KY209956, KY210080, KY210121, –; Blepharispermum villosum O. Hoffm., Ethiopia, Anderberg 1729 (S), KY209959, KY210082, KY210123, KY210042; Blepharispermum xerothamnum Mattf., Tanzania, Greenway & Polhill 11709 (S), KY209958, –, –, KY210041; Blepharispermum zanguebaricum Oliv. & Hiern, Tanzania, Eriksson & al. 571 (S), KY209957, KY210081, KY210122, KY210040; Callilepis salicifolia Oliv., South Africa, Bayer & al. SAF-01009 (S), LN606837, LN607423, AY780851.2, LN607070; Centipeda cunninghamii (DC.) A. Braun & Asch., New Zealand, de Lange s.n. (S), KY209960, KY210083, KY210124, KY210043; Centipeda minima (L.) A. Braun & Asch., Japan, Anderberg & Lundin 58 (S), HE862168, KY210084, HE862354, HE974693; Centipeda racemosa (Hook.) F. Muell., Australia, Walsh 4976 (MEL), HE862197, HE862069, HE862379, HE974722; Centipeda thespidioides F. Muell., Australia, Weber 2981 (S), KY209961, KY210085, KY210125, KY210044; Dittrichia viscosa (L.) Greuter, Greece, Trift & al. 22 (S), –, EF210966, LN607622, EF211061; Inula aschersoniana Janka, Greece, Rechinger 45149 (S), –, FM995373, FM208933, FM997845; Leucoblepharis subsessilis Arn., India, Yadav 2342 (S), KY209951, KY210075, KY210116, KY210034; Lowryanthus rubens Pruski, Madagascar, Antilahimena & al.4801 (S S08-80), KY209962, KY210086, KY210126, KY210045; Lowryanthus rubens, Madagascar, Razakamalala & al. 2369 (S S08-79), KY209963, KY210087, KY210127, KY210046; Pulicaria aucheri Jaub. & Spach, Iran, Sojak 4947 (S), –, FM995393, FM208991, FM997867; Rochonia cinerarioides DC., Madagascar, Razafimandimbison 2858 (S S20-19232), –, –, OQ427099*, –; Symphyllocarpus exilis Maxim., Russia, Antonova s.n. (S), KY209967, KY210091, KY210131, KY210050; Vernoniopsis caudata (Drake) Humbert, Madagascar, Ratovoson 1918 (MO MO6590064), OQ410985*, OQ429286*, OQ427107*, OQ410998*; Vernoniopsis caudata, Madagascar, Razafimandimbison, Razafindrahaja, Atahaly & Swenson 1448 (MO MO6840514), OQ410986*, OQ429287*, OQ427106*, OQ410999*; Vernoniopsis lokohensis (Humbert) Callm. & Phillipson, Madagascar, Razafimandimbison & Razafindrahaja 2969 (S S20-19251), OQ410977*, OQ429278*, OQ427100*, OQ410990*; Vernoniopsis lokohensis, Madagascar, Miller & Lowry 4132 (MO MO04870174), OQ410984*, OQ429285*, –, OQ410997*.
Additional ndhF sequences: Achillea millefolium L. (Anthemideae), L39442; Acourtia microcephala DC. (Nassauvieae), L39407, L39408; Adenocaulon himalaicum Edgew. (Mutisieae), L39466; Ainsliaea acerifolia Sch. Bip. (Pertyeae), L39410; Ambrosia trifida L. (Heliantheae), L39382; Anastraphia parvifolia Britton (Gochnatieae), L39397; Anisothrix integra (Compton) Anderb. (Gnaphalieae), L39437; Antennaria howellii Greene (Gnaphalieae), L39436; Arctotis stoechadifolia P. J. Bergius (Arctotideae), L39425; Atractylodes japonica Koidz. ex Kitam. (Cardueae), L39413; Baccharis neglecta Britton (Astereae), L39448; Bahia absinthifolia Benth. (Bahieae), L39464; Barnadesia caryophylla S. F. Blake (Barnadesieae), L39394; Bellis perennis L. (Astereae), L39446; Blennosperma nanum (Hook.) S. F. Blake (Senecioneae), L39433; Boopis anthemoides Juss. (Calyceraceae), L39384; Calendula officinalis L. (Calenduleae), L39439; Carlina vulgaris L. (Cardueae), L39412; Carthamus tinctorius L. (Cardueae), L39417; Centaurea americana Nutt. (Cardueae), L39416; Chromolaena sp. (Eupatorieae), L39375; Chrysanthemum morifolium Ramat. (Anthemideae), L39443; Chuquiraga jussieui J. F. Gmel. (Barnadesieae), L39393; Cichorium intybus L. (Lactuceae), L39390; Cirsium arvense (L.) Scop. (Cardueae), L39419; Cirsium texanum Buckley (Cardueae), L39418; Conyza sp. (Astereae), L39451; Coreopsis tinctoria Nutt. (Coreopsideae), L39461; Cosmos bipinnatus Cav. (Coreopsideae), L39462; Coulterella capitata Vasey & Rose (Tageteae), L39380; Dahlia coccinea Cav. (Coreopsideae), L39460; Dasyphyllum argenteum Kunth (Barnadesieae), L39392; Delairea odorata Lem. (Senecioneae), L39435; Dimorphotheca pluvialis (L.) Moench (Calenduleae), L39438; Dipterocome pusilla Fisch. & C. A. Mey. (Cardueae), FJ813488; Doniophyton anomalum (D. Don) Kurtz (Barnadesieae), L39396; Echinops exaltatus Schrad. (Cardueae), L39411; Eremothamnus marlothianus O. Hoffm. (Arctotideae), L39424; Eupatorium atrorubens (Lem.) N. E. Br. (Eupatorieae), L39376; Feddea cubensis Urb. (Feddeeae), EF089566; Felicia bergeriana (Spreng.) O. Hoffm. (Astereae), L39445; Fitchia sp. (Coreopsideae), L39459; Flaveria ramosissima Klatt (Tageteae), L39465; Gazania splendens Lem. (Arctotideae), L39423; Geigeria acaulis O. Hoffm. (Inuleae), LN607711; Geraea canescens Torr. & A. Gray (Heliantheae), L39381; Gerbera jamesoniiAdlam (Mutisieae), L39403; Gerbera piloselloides (L.) Cass. (Mutisieae), L39404; Gutenbergia polytrichomata Wech. (Vernonieae), L39429; Gymnanthemum capense (A. Spreng.) J. C. Manning & Swelank. (Vernonieae), L39427; Haplocarpha scaposa Harv. (Arctotideae), L39426; Helianthus annuus L. (Heliantheae), L39383; Inula germanica L. (Inuleae), LN607649; Jasonia tuberosa (L.) DC. (Inuleae), AY780844; Jaumea carnosa (Less.) A. Gray (Tageteae), L39378; Lactuca sativa L. (Lactuceae), L39389; Leibnitzia anandria (L.) Turcz. (Mutisieae), L39402; Lopholaena coriifolia (Sond.) E. Phillips & C. A. Sm. (Senecioneae), L39434; Lychnophora tomentosa (Mart. ex DC.) Sch. Bip. (Vernonieae), L39428; Madia elegans D. Don ex Lindl. (Madieae), L39374; Marshallia caespitosa Nutt. ex DC. (Helenieae), L39458; Munnozia gigantea (Rusby) Rusby (Liabeae), L39420; Mutisia acuminata Ruiz & Pav. (Mutisieae), L39400; Nassauvia gaudichaudii (Cass.) Cass. (Nassauvieae), L39405; Onoseris hyssopifolia Kunth (Onoserideae), L39398; Oritrophium peruvianum (Lam.) Cuatrec. (Astereae), L39450; Osteospermum muricatum E. Mey. ex DC. (Calenduleae), L39440; Palafoxia arida B. L. Turner & M. I. Morris (Bahieae), L39463; Piptocarpha axillaris (Less.) Baker (Vernonieae), L39431; Pluchea obovata Balf. f. (Inuleae), LN607671; Psilostrophe gnaphalodes DC. (Helenieae), L39457; Pyrrocoma sp. (Astereae), L39447; Rosenia humilis (Less.) K. Bremer (Gnaphalieae), AF063080; Santolina chamaecyparissus L. (Anthemideae), L39444; Saussurea eriophylla Nakai (Cardueae), L39414; Schlechtendalia luzulifolia Less (Barnadesieae), L39395; Sinclairia glabra (Hemsl.) Rydb. (Liabeae), L39421; Sinclairia pringlei (B. L. Rob. & Greenm.) H. Rob. & Brettell (Liabeae), L39422; Stifftia chrysantha J. C. Mikan (Stifftieae), L39399; Stokesia laevis (Hill) Greene (Vernonieae), L39430; Symphyotrichum cordifolium (L.) G. L. Nesom (Astereae), L39449; Syneilesis palmata (Thunb.) Maxim. (Senecioneae), L39432; Synurus deltoides (Aiton) Nakai (Cardueae), L39415; Tagetes erecta L. (Tageteae), L39466; Tarchonanthus camphoratus L. (Tarchonantheae), L39409; Thymophylla pentachaeta (DC.) Small (Tageteae), L39467; Tragopogon porrifolius L. (Lactuceae), L39391; Trixis californica Kellogg (Nassauvieae), L39406; Ursinia nana DC. (Anthemideae), L39441; Venegasia carpesioides DC. (Madieae), L39379; Verbesina robinsonii (Klatt) Fernald ex B. L. Rob & Greenm. (Heliantheae), L39377.
Supplemental content online
See https://doi.org/10.3372/wi.54.54107
Supplementary appendix S1 (wi.54.54107_Supplementary_appendix_S1_ndhF_matrix.nex). DNA ndhF sequence alignment in nexus format.
Supplementary appendix S2 (wi.54.54107_Supplementary_appendix_S2_combined_matrix.nex). DNA sequence alignment in nexus format for the combined dataset.
