EMBRYOPSIDA Pirani & Prado (crown group)

Gametophyte dominant, independent, multicellular, thalloid, with single-celled apical meristem, showing gravitropism; flavonoids + [absorbtion of UV radiation]; protoplasm dessication tolerant [plant poikilohydric]; cuticle +; cell walls with (1->4)-ß-D-glucans [xyloglucans], lignin +; rhizoids unicellular; several chloroplasts per cell; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles in vegetative cells 0, metaphase spindle anastral, predictive preprophase band of microtubules, phragmoplast + [cell wall deposition spreading from around the spindle fibres], plasmodesmata +; antheridia and archegonia jacketed, stalked; spermatogenous cells monoplastidic, centrioles develop de novo, associated with basal bodies of flagellae, multilayered structure +, proximal end of basal bodies lacking symmetry, stellate pattern associated with doublet tubules of transition zone; spermatozoids with a left-handed coil; male gametes with 2 lateral flagellae; oogamy; diploid embryo initially surrounded by haploid gametophytic tissue, plane of first division horizontal [with respect to long axis of archegonium/embryo sac], suspensor/foot +, cell walls with nacreous thickenings; sporophyte multicellular, sporangium +, single, with polar transport of auxin, dehiscence longitudinal; meiosis sporic, monoplastidic, microtubule organizing centre associated with plastid, cytokinesis simultaneous, preceding nuclear division, sporocytes 4-lobed, with a quadripolar microtubule system; spores in tetrads, sporopollenin in the spore wall, wall with several trilamellar layers [white-line centred layers, i.e. walls multilamellate]; spores trilete [?level]; close association between the trnLUAA and trnFGAA genes on the chloroplast genome.

Note that many of the bolded characters in the characterization above are apomorphies in the streptophyte clade along the lineage leading to the embryophytes rather than being apomorphies of the embryophytes.

STOMATOPHYTES

Abscisic acid, ?D-methionine +; sporangium with seta, seta developing from basal meristem [between epibasal and hypobasal cells], sporangial columella + [developing from endothecial cells]; stomata +, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and in rhizoids/root hairs; polar transport of auxins and class 1 KNOX genes expressed in the sporangium alone; MIKC, MI*K*C* and class 1 and 2 KNOX genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns.

[Hornworts + Polysporangiophyta]: archegonia embedded/sunken in the gametophyte; sporophyte long-lived, chlorophyllous, nutritionally largely independent of the gametophyte; sporophyte-gametophyte junction interdigitate, sporophyte cells showing rhizoid-like behaviour; spores trilete.

POLYSPORANGIOPHYTA

Sporophyte well developed, branched, free living, sporangia several; spore walls not multilamellate [?here]; apical meristem +.

EXTANT TRACHEOPHYTA / VASCULAR PLANTS

Photosynthetic red light response; water content of protoplasm relatively stable [plant homoiohydric]; control of leaf hydration passive; (condensed or nonhydrolyzable tannins/proanthocyanidins +); vascular tissue +, sieve cells + [nucleus degenerating], tracheids +, in both protoxylem and metaxylem; endodermis +; root xylem exarch [development centripetal]; stem with an apical cell; branching dichotomous; leaves spirally arranged, blades with mean venation density 1.8 mm/mm2 [to 5 mm/mm2]; sporangia adaxial on the sporophyll, sporangia derived from periclinal divisions of several epidermal cells, wall multilayered [eusporangium]; columella 0; stellate pattern split between doublet and triplet regions of transition zone; placenta with single layer of transfer cells in both sporophytic and gametophytic generations, embryo with roots arising lateral to the main axis [plant homorhizic].

[MONILOPHYTA + LIGNOPHYTA]

Branching ± monopodial; lateral roots +, endogenous, root apex multicellular, root cap +; tracheids with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangia borne in pairs and grouped in terminal trusses, dehiscence longitudinal, a single slit; cells polyplastidic, microtubule organizing centres not associated with plastids, diffuse, perinuclear; male gametes multiflagellate, basal bodies staggered, blepharoplasts paired; chloroplast long single copy ca 30kb inversion [from psbM to ycf2].

LIGNOPHYTA

Plant woody; lateral root origin from the pericycle; shoot apical meristem multicellular; branching lateral, meristems axillary; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].

EXTANT SEED PLANTS/SPERMATOPHYTA

Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins derived from (some) sinapyl and particularly coniferyl alcohols [hence with p-hydroxyphenyl and guaiacyl lignin units, so no Maüle reaction]; root with xylem and phloem originating on alternate radii, vascular tissue not medullated, cork cambium deep seated; arbuscular mycorrhizae +; shoot apical meristem interface specific plasmodesmatal network; stem with vascular cylinder around central pith [eustele], phloem abaxial [ectophloic], endodermis 0, xylem endarch [development centrifugal]; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; stem cork cambium superficial; branches exogenous; leaves with single trace from vascular sympodium [nodes 1:1]; stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; leaves with petiole and lamina, development basipetal, blade simple; axillary buds +, not associated with all leaves; prophylls two, lateral; plant heterosporous, sporangia borne on sporophylls; microsporophylls aggregated in indeterminate cones/strobili; true pollen +, grains mono[ana]sulcate, exine and intine homogeneous; ovules unitegmic, parietal tissue 2+ cells across, megaspore tetrad linear, functional megaspore single, chalazal, lacking sporopollenin, megasporangium indehiscent; pollen grains landing on ovule; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, gametes two, developing after pollination, with cell walls; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large" [ca 8 mm3], but not much bigger than ovule, with morphological dormancy; embryo cellular ab initio, endoscopic, plane of first cleavage of zygote transverse, suspensor +, short-minute, embryo axis straight, so shoot and root at opposite ends [plant allorhizic], white, cotyledons 2; plastid transmission maternal; ycf2 gene in inverted repeat, whole nuclear genome duplication [zeta duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], nrDNA with 5.8S and 5S rDNA in separate clusters; mitochondrial nad1 intron 2 and coxIIi3 intron and trans-spliced introns present.

MAGNOLIOPHYTA

Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANITA grade?], S [syringyl] lignin units common [positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, exodermis +; shoot apex with tunica-corpus construction, tunica 2-layered; reaction wood ?, associated gelatinous fibres [g-fibres] with innermost layer of secondary cell wall rich in cellulose and poor in lignin; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, cytoplasm not occluding pores of sieve plate, companion cell and sieve tube from same mother cell; sugar transport in phloem passive; nodes 1:?; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance to increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, venation hierarchical-reticulate, secondary veins pinnate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; most/all leaves with axillary buds; flowers perfect, pedicellate, ± haplomorphic, parts spiral [esp. the A], free, numbers unstable, development in general centripetal; P +, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], ± embedded in the filament, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally, endothecium +, endothecial cells elongated at right angles to long axis of anther; tapetum glandular, cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine thin, compact, lamellate only in the apertural regions; nectary 0; carpels present, superior, free, several, ascidiate, with postgenital occlusion by secretion, stylulus short, hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry [not secretory]; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across [crassinucellate], nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; supra-stylar extra-gynoecial compitum +; ovule not increasing in size between pollination and fertilization; pollen grains landing on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollination siphonogamous, tube elongated, growing between cells, growth rate 20-20,000 µm/hour, outer wall pectic, inner wall callose, with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, flagellae 0, double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; seed exotestal, becoming much larger than ovule at time of fertilization; endosperm diploid, cellular [micropylar and chalazal domains develop differently, first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous; embryogenesis cellular; dark reversal Pfr -> Pr; Arabidopsis-type telomeres [(TTTAGGG)n]; 2C genome size 1-8.2 pg [1 pg = 109 base pairs], whole nuclear genome duplication [epsilon duplication]; protoplasm dessication tolerant [plant poikilohydric]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]].

[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.

[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood +; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; carpels plicate; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.

[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [possible position]; pollen tube growth intra-gynoecial; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.

[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).

[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.

EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessels with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; K/outer P members with three traces, ("C" +, with a single trace); A few, (polyandry widespread, initial primordia 5, 10, or ring, ± centrifugal), filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?

[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).

[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.

[BUXALES + CORE EUDICOTS]: ?

CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one place]; micropyle?; whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.

[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls developing internally/adaxially to the corolla whorl and successively alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G [5], G [3] also common, when [G 2], carpels superposed, compitum +, placentation axile, style +, stigma not decurrent; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression.

[SANTALALES [BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?

[BERBERIDOPSIDALES [CARYOPHYLLALES + ASTERIDS]]: ?

[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.

ASTERIDS / Sympetalae redux? / ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate, if evident only early in development and then petals often appearing to be free); anthers dorsifixed?; (nectary gynoecial); style +, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal cells lignified, esp. on anticlinal and/or inner periclinal walls; endosperm cellular.

[ERICALES [ASTERID I + ASTERID II]]: (ovules lacking parietal tissue) [tenuinucellate].

[ASTERID I + ASTERID II] / CORE ASTERIDS: ellagic acid 0, non-hydrolysable tannins not common; sugar transport in phloem active; inflorescence basically cymose; A = and opposite sepals or P, (numerous, usu. associated with increased numbers of C or G); (pollen with orbicules); style short[?]; duplication of the PI gene.

ASTERID II / CAMPANULIDAE: myricetin 0; vessel elements with scalariform perforation plates; flowers rather small; endosperm copious, embryo short/very short.

[ASTERALES [ESCALLONIALES [BRUNIALES [APIALES [PARACRYPHIALES + DIPSACALES]]]]] / APIIDAE: iridoids +; C forming a distinct tube, tube initiation early; A epipetalous; ovary inferior, [2-3], style long[?].

Age. Magallón and Castillo (2009) offer estimates of 96-94 m.y. for crown-group ages, Bremere et al. (2004: note topology) an age of ca 114 m.y., Bell et al. (2010: also note topology) ages of (94-)84, 77(-69) m.y., N. Zhang et al. (2012) suggested ages of (89-)74(-52) m.y., Xue et al. (2012) an age of 67.3-64.2 m.y., Naumann et al. (2013) an age of around 82.9 m.y., while Beaulieu et al. (2013a: 95% HPD) estimated an age of (109-)99(-89) m.y..

Divergence & Distribution. Divergence at this node probably occurred in plants growing in the southern hemisphere (Beaulieu et al. 2013a).

Endress (2011a) suggested that the inferior ovary so common here (but there are reversals) might be a key innovation.

Chemistry, Morphology, etc. Polyacetylenes are sporadic in this clade, occurring in Asterales, Dipsacales and Apiales, but always in much embedded clades. Although usually not occurring with iridoids in the one plant, the two may sometimes be found together, as in Torricellia angulata (Pan et al. 2006; Liang et al. 2009). Given the rather strongly supported set of relationships at the base of Apiales, the other clades that are in this part of the asterid II phylogeny, and relationships within Asterales (Campanulaceae s.l. and Asteraceae are not immediately related), these similarities are probably parallelisms.

The position of early initiation of the corolla tube on the tree is quite uncertain. Although a number of families in this clade have members with such initiation, not only is sampling within the larger orders poor and the smaller orders largely non-existent, in the asterid I group both Oleaceae and Rubiaceae, "basal" or almost so in their orders, may have early initiation. Corolla initiation in Garryales and associated families is unknown (Leins & Erbar 2003b for a summary). There may be a developmental connection between early corolla tube formation and the way inferior ovaries in the asterid II clade develop. (Ronse Decraene & Smets 2000). Although the character "ovary inferior" can be placed at this level on the tree, there are frequent reversals to "ovary superior" (see Apiales); whether corolla development changes accordingly is of some interest.

The I copy of the RPB2 gene is lost in most members of this clade (Oxelman et al. 2004; Luo et al. 2007), but it occurs both in Escalloniaceae and Apiales. However, clades like Paracryphiales and Bruniales (Lundberg 2001e) have not been sampled for this gene.

Previous Relationships. There are some phytochemical similarities between the clade [Pittosporaceae [Araliaceae [Myodocarpaceae + Apiaceae]]] and some Asterales (esp. Campanulaceae s.l. and Asteraceae) (e.g. Erbar & Leins 2004; Leins & Erbar 2004b).

ASTERALES Link  Main Tree.

(Route I secoiridoids, oligo- or polyfructosans, inc. inulin, with isokestose linkages [starch generally 0] +); apotracheal parenchyma 0; leaves spiral; flower size?; C valvate, petal apiculi inflexed; A (basifixed), free from C; pollen grains trinucleate; nectary +; style long; ovules many/carpel, integument <7 cells thick, endothelium +, hypostase 0; antipodal cells ephemeral; embryo suspensor filamentous, micropylar and chalazal endosperm haustoria +; mitochondrial rpl2 gene lost. - 11 families, 1743 genera, 26,870 species.

Age. Wikström et al. (2001) suggested an age of (95-)90, 83(-77) m.y. for the crown group, Bremer et al. (2004) around 93 m.y., while estimates in Janssens et al. (2009) are rather older - 94±11.2 m.y. old. Magallón and Castillo (2009) estimate an age of (84.7-)84.5, 84.3(-84.1) m.y., Beaulieu et al. (2013a: 95% HPD) thought that the crown clade was (101-)89(-79) m.y. old.

Note: Possible apomorphies are in bold. However, the actual level at which many of these features, particularly the more cryptic ones, should be assigned is unclear. This is partly because many characters show considerable homoplasy, in addition, basic information for all too many is very incomplete, frequently coming from taxa well embedded in the clade of interest and so making the position of any putative apomorphy uncertain. Then there is the not-so-trivial issue of how ancestral states are reconstructed...

Divergence & Distribution. Asterales contain ca 13.6% eudicot diversity (Magallón et al. 1999). The clade is characterised by having notably small seeds (Moles et al. 2005a; Sims 2012).

Movemenent into the northern hemisphere of Asterales may be linked with the origin of hyperdiverse clades like Asteraceae and Campanulaceae (Beaulieu et al. 2013a), although the basic topology of relationships in Campanulaceae is still unclear and there are suggestions that diversification in Asteraceae began in South America (see that family).

Endress (2011a) thought that the character "monosymmetric flower" in Asterales might be a key innovation, although where it is to be placed on the tree is unclear. Somewhere near the speciose Campanulaceae-Lobelioideae will represent one acquisition of this feature, a position near Asteraceae another. Furthermore, although monosymmetric flowers may occur in most Asteraceae, the capitulum itself is polysymmetric or haplomorphic, and major pollinators behave accordingly (see below under Asteraceae). Endress (2011a) also suggested that a key innovation somewhere in Asterales was tenuinucellate ovules. Unfortunately, corolla and endosperm development, endothelium presence, not to mention chemistry (for a partial summary, see Grayer et al. 1999), etc., are unknown in some critical families, so understanding character evolution is particularly difficult. Absence of apotracheal parenchyma and x = 9 may also be features of Asterales (Lundberg & Bremer 2001; Bremer et al. 2001).

Pollination Biology. Several families, notably Campanulaceae and the Asteraceae area, have forms of secondary pollen presentation (Carolin 1960b; Erbar & Leins 1995a; Leins 2000; Leins & Erbar 1997, Erbar 2003b: Yeo 1993 for a general summary), and Leins (2000) and Leins and Erbar (2006, 2010) in particular discuss in considerable detail the evolution of these pollen presentation mechanisms.

Ecology & Physiology. Fructans may stabilize cell membranes under drought and/or freezing conditions (Livingston III et al. 2009).

Chemistry, Morphology, etc. The corolla lobes quite often appear to consist of a central portion and marginal "wings" reflecting the induplicate-valvate corolla aestivation of such flowers. For a study of petal vasculature, which shows interesting variation, see Gustafsson (1995). Monosymmetry is often associated with a slit the length of the corolla. Variation of ovary position in Asterales is considerable.

Tobe and Morin (1996) summarize embryological knowledge of many members of the order. For some inflorescence morphology, see Philipson (1953), for fructans/inulins, see Meier and Reid (1982), for integument thickness, see Inoue and Tobe (1999), for some inflorescence development, see Harris (1999), and for pollen, see Polevova (2006). For a general discussion of variation in the order, see J. Kadereit (2006) and Lundberg (2009).

Phylogeny. Extsensive phylogenetic structure in Asterales, although often with rather weak support, was early apparent (D. Soltis et al. 2000; see also Olmstead et al. 2000). Subsequent studies improved support for many clades, although there was still a basal polytomy (Kårehed et al. 2000; Lundberg 2001a, b; Kårehed 2002a; especially Bremer et al. 2001; Lundberg & Bremer 2001, 2003). Olmstead et al. (2000) and B. Bremer et al. (2002) suggested a sister group relationship between Campanulaceae and Stylidiaceae (but not Donatia), and the latter authors suggest that Pentaphragmataceae are also linked to this clade; Donatia itself is there very weakly linked with Alseuosmiaceae et al. Stylidiaceae and Donatiaceae are associated as weakly supported sister taxa (D. Soltis et al. 2000) or quite strongly linked (Kårehed et al. 2000; Lundberg 2001; Tank & Donoghue 2010); in some studies Donatiaceae are sister to Abrophyllum (Carpodetaceae: Gustafsson et al. 1997), not to Stylidiaceae. There were suggestions that Rousseaceae, Pentaphragmataceae and Campanulaceae are together sister to the other Asterales (Lundberg & Bremer 2003), although the support was not very strong, while Soltis et al. (2007a) found Campanulaceae to be sister to rest of Asterales (1.0 p.p.). Rousseaceae s.l. are often found to be sister to Campanulaceae (Kårehed 2002a; Tank et al. 2007; esp. Tank & Donoghue 2010), but Bell et al. (2010) found Roussea to be sister to the rest of the order. Relationships between Asteraceae and its immediate relatives also vary somewhat according to the gene studied (A.P.G. 2003 for references), while Soltis et al. (2011) found that Pentaphragmataceae were sister to all other Asterales, but with little support - and perhaps because of the pull of some mitochondrial genes. However, relationships along the spine of Asterales were quite well resolved in a ten chloroplast gene analysis of Tank and Donoghue (2010) and are followed here; Soltis et al. (2011) found a largely similar topology, apart from the position of Pentaphragmataceae and a weakly supported set of relationships [Phellinaceae [Alseuosmiaceae + Argophyllaceae]].

Stylidiaceae and Donatiaceae have often been associated, e.g. as weakly supported sister taxa (D. Soltis et al. 2000) or quite strongly linked (Kårehed et al. 2000; Lundberg 2001). In some studies Donatiaceae are sister to Abrophyllum (Carpodetaceae: Gustafsson et al. 1997), not to Stylidiaceae.

Previous Relationships. Asterales are basically Takhtajan's (1997) Asteridae, with the addition of sundry Hydrangeales. Cronquist (1981) also included many families here included in Asterales in the orders placed towards the end of his Asteridae, although some families were also included in Cornales (Rosidae), etc.



Includes Alseuosmiaceae, Argophyllaceae, Asteraceae, Calyceraceae, Campanulaceae, Goodeniaceae, Menyanthaceae, Pentaphragmataceae, Phellinaceae, Rousseaceae, Stylidiaceae.

Synonymy: Alseuosmiineae Reveal - Alseuosmiales Doweld, Ambrosiales Dumortier, Anthemidales Link, Boopidales Berchtold & J. Presl, Brunoniales Lindley, Calendulales Link, Calycerales Link, Campanulales Berchtold & J. Presl, Carduales Small, Cichoriales Link, Cynarales Rafinesque, Echinopales Link, Goodeniales Berchtold & J. Presl, Lobeliales Link, Menyanthales J. Presl, Pentaphragmatales Doweld, Phellinales Doweld, Rousseales Doweld, Scaevolales Martius, Stylidiales Berchtold & J. Presl

[Rousseaceae + Campanulaceae]: A free.

Age. Wikström et al. (2001) suggested an age of (86-)81, 76(-71) m.y. for this node.

ROUSSEACEAE Candolle   Back to Asterales

Rousseaceae

Young stem with separate bundles; lamina margins gland-toothed; inflorescence terminal; G [5], mostly superior, opposite petals; integument 5-8 cells across.

4[list]/13 - two subfamilies below. Mauritius, scattered from New Guinea to New Zealand.

1. Rousseaoideae

Evergreen climber to small tree; chemistry?, tannins 0; cork?; resin canals +; petiole bundle cylindrical; buds perulate; hairs tufted-stellate and glandular-peltate; leaves opposite, leaf base broad; flowers single; flowers large, (4-merous), K valvate, C connate; anthers basifixed, attached their entire length to stout connective, sagittate, extrorse; pollen 6- or 8-porate, tectum complete; G [5-7], style expanding apically, stigmatic lobes narrower, erect; ovule ?bitegmic; fruit a berry, K persistent; seed coat with thick-walled exotesta, the rest crushed; micropylar haustorium +, embryo medium-long; n = ?

1/1: Roussea simplex. Mauritius (see Map above: green). [Photo - Flower © D. Lorence]

2. Carpodetoideae J. Lundberg

Trees; chemistry?; petiole bundles arcuate or annular plus accessories; hairs unicellular, thick-walled, strongly curved, warty; inflorescence paniculate; flowers small, 4-6-merous; C becoming free; A attachment?; (pollen in tetrads - Carpodetus); G [3-6], style short (0), stigma capitate (± divided - Cuttsia); fruit dry, baccate, or a loculicidal + septicidal capsule, K deciduous; seeds many, funicle elongated, exotestal cells massively thickened on anticlinal and inner periclinal walls (all around - Carpodetus); endosperm hemicellulosic [Carpodetus], ?haustoria; embryo?; n = 14, 15.

3/12. New Zealand, E. Australia, Papuasia (see Map above: red). [Photo - Inflorescence.]

Synonymy: Abrophyllaceae Nakai, Carpodetaceae Fenzl

Evolution. Pollination Biology. Roussea is pollinated by a gecko (the pollen is embedded in a slimy substance), which may also disperse its seeds (Hansen & Müller 2009.

Chemistry, Morphology, etc. Roussea in particular is poorly known. It has an endodermis in its petiole, and its seed is drawn as if it were carunculate (Engler 1930a). Mauritzon (1933) suggested that it might have bitegmic ovules. For a summary of what little is known about the plant, see Koontz et al. (2006).

Abrophyllum and Cuttsia both have clusters of small, unlignified cells in the mesophyll that look like little white raphide bundles (Hils 1985). For a useful summary, see Gustafsson (2006).

Details of vegetative anatomy of Carpodetoideae are taken from Hils (1985), of indumentum from Al-Shammary and Gornall (1994), of floral morphology from Tobe and Raven (1999), and of seed anatomy from Takhtajan (2000). For anatomy of Roussea, see Watari (1939) and Ramamonjiarisoa (1980), also Mauritzon (1933: ovules); for the wood anatomy of some Carpodetoideae, see Carlquist (2012c). For general anatomy, see Gornall et al. (1998), for some general information, see Gustaffson and Bremer (1997).

Phylogeny. For the circumscription of the family, see Lundberg (2000a).

Previous Relationships. Rousseaceae were previously of uncertain position. Thus Takhtajan (1997) placed them in Rosidae-Celastranae-Brexiales, and they have often been associated with Saxifragaceae s.l.; (see summary in Lundberg 2001a). The anthers in particular are quite unlike those of ex-Saxifragaceae, especially Escalloniaceae (see Escalloniales here) that are otherwise somewhat similar to Rousseaceae. Carpodetaceae, another group often thought of as "woody saxifrages", were included in Hydrangeales by Takhtajan (1997). None of these genera was mentioned by Cronquist (1981), which was perhaps wise.

CAMPANULACEAE Jussieu, nom. cons.   Back to Asterales

Herbs, whether annual or perennial, to shrubs and pachycaul rosette plants; inulin +, polyacetylenes + [14-C aliphatic tetrahydropyran derivatives], iridoids and tannins 0, little oxalate accumulation; cork also inner cortical; vascular cylinder +; (medullary vascular bundles +); vessel elements with simple perforation plates; nodes 1:1; articulated laticifers +; crystals acicular; petiole bundles incurved-arcuate; leaves (opposite), lamina vernation variable, margins entire to toothed (lobed), hydathodes common; inflorescence terminal, racemose; flowers (3-)5(-10)-merous; median K abaxial, C with early tube formation, connate; secondary pollen presentation + [flowers protandrous, A basifixed, anthers introrse, at least initially close to stigma, connivent when dehiscing, dehiscence in bud, style elongating subsequently]; pollen (binucleate), endexine throughout, not lamellate; G [2(-5)], (± superior), (placentation parietal), placentae intrusive, bilobed, style elongating after A dehiscence, with hairs, stigma lobed; integument ca 6 cells across; fruit a loculicidal capsule, K persistent; seeds many, exotesta cells lignified, polygonal or elongated, (endotestal cells, esp. inner walls, thickened); endosperm (starchy), copious; expansion of chloroplast inverted repeat into small single copy region, 5bp ndhF deletion, chloroplast infA and accD genes lost [but see Haberle et al. 2008a], biparental plastid transmission [?levels], mitochondrial coxII.i3 intron 0.

84[list]/2380. World-wide - five subfamilies below.

Age. Bell et al. (2010: Campanuliodeae + Lobelioideae) estimated a crown group age of (67-)56, 53(-41) m.y. for the family and Wikström et al. (2001) suggested an age of (62-)59, 46(-43) m.y..

[Nemocladoideae + Campanuloideae]: pollen spheroid to oblate-spheroid, verrucate or with spicules; fibrillar protein bodies in nuclei.

Nemacladoideae

1. Nemacladoideae M. H. G. Gustafsson

Tiny annuals (one perennial); flowers small, ± monosymmetric; C polysymmetric or monosymmetric, 3;2; A (adnate to C), fimbriate "scales" at outside bases of adaxial filaments where they join the C, filaments free basally, connate apically, (anthers spreading), free; pollen tricolporate or 6-colpate; large "glands" at base of style; G also [3], half inferior to superior, style head presenting pollen, bending towards or away from median K; ?embryology; (fruit circumscissile - N. californicus); n = 9.

2/25: Nemacladus (24). S.W. U. S. A., esp. California, Mexico (map: from Wimmer 1968).

Synonymy: Nemacladaceae Nuttall

2. Campanuloideae Burnett Campanuloideae

Perennials (annuals), roots often thick; caffeic acid, p-coumaric acid, latex rich in polysterols; (vessel elements with scalariform perforation plates); palisade mesophyll with arm cells; inflorescence often ± cymose; flowers large, polysymmetric; median K adaxial; stamens sprawling at bottom of corolla tube after anthers have dehisced, bases conceal nectar; pollen echinate; G (1 [2) 3-5(-10)], opposite sepals (C), or median member adaxial, style (hollow - how common?), long-hairy, especially in the upper half or so, hairs with bulbous bases, retractile, presenting pollen, stigma dry or wet; (integument 8-11 cells across, vascularized, podium not persistent, placental obturator + - Azorina); chalazal haustorium single-celled, (embryo medium); (fibrillar protein intranuclear inclusions); extensive rearrangements in the chloroplast inverted repeat.

50/1050. More or less world-wide, but few in Australia-New Zealand and South Americar (map: from Hultén 1971; Thulin 1975; Shulkina 1978; FloraBase v.2011).

Age. Estimates of the age of this node are (48-)45, 33(-30) m.y. (Wikström et al. 2001) and (56-)43, 41(-28) m.y. (Bell et al. 2010).

2A. Ostrowskieae Fedorov

Leaves often opposite; (A 3); pollen colpate/colporate; G [5], opposite ?; (fruit a berry); n = 7-9 (17).

4/60: Codonopsis (30), Cyananthus (23). Central Asia to West Malesia, few in Canaries and Africa, often (sub)tropical, not Europe or northern Asia.

2B. Campanuleae Dumortier/Wahlenbergieae

(Leaves opposite); (A adnate to C); pollen porate, (flattened-triangular); fruit also dehiscing down sides by pores or slits [caused by activity of axicorn on drying - Campanuleae, inc. Edraianthus]; n = 6+ [17 common]; epicotyl and hypocotyl usually not elongated.

46[notional]/975: Campanula (420), Wahlenbergia (260), Adenophora (65). Especially N. temperate Old World, very few in the Australia-New Zealand area.

Synonymy: Cyananthaceae J. Agardh, Jasionaceae Dumortier

[Lobelioideae + Cyphocarpoideae + Cyphioideae]: flowers monosymmetric; pollen prolate; stylar tip at base of opening anthers, hairs only at tip of style.

Lobelioideae

3. Lobelioideae Burnett

(Annuals) perennials, herbs to small trees; chelidonic acid, pyr[roliz]idine alkaloids +, p-coumaric acid, caffeic acid 0; lamina vernation supervolute [Lobelia]; flowers large to small, resupinate by pedicel torsion, (not); C (3:2), 2:3, 0:5 [split-monosymmetric], (spurred - Heterotoma); filaments connate at least apically, anthers connate; pollen reticulate-striate; style with brush hairs, pollen in pollen box [pump mechanism: Nüdelspritze], stigma wet; synergids hooked, (antipodal cells barely persistent); (fruit a berry; a circumscissile capsule; dehiscing down its inferior part); n = (6-)7(-13).

29/1200: Lobelia (400+), Siphocampylus (230+), Centropogon (215), Burmeistera (100+), Cyanea (80). Almost world-wide, not Arctic and absent from the Near East and central Asia, largely tropical, especially common in the New World (map: see Wimmer 1943; Meusel & Jäger 1992; FloraBase 2007). [Photo - Flower, Fruit.]

Age. Ages for diversification within Lobelioideae differ greatly according to how they are estimated - e.g. (59.6-)54.9(-50.9) m.y. (penalized likelihood) versus (88.2-)72.7(-52.2) milion years (BEAST: see Antonelli 2009).

Synonymy: Dortmannaceae Ruprecht, Lobeliaceae Jussieu, nom. cons.

Cyphocarpoideae

4. Cyphocarpoideae Gustafsson

Annual to perennial herbs; leaves deeply lobed; C induplicate-valvate, 1:4, adaxial petal cucullate, with apical appendage; A epipetalous, free; ovary notably elongated; ?embryology; fruit dehiscing through sides; n = 9; nuclear inclusions fibrillar.

1/3. Chile.

Synonymy: Cyphocarpaceae Reveal & Hoogland

5. Cyphioideae Schönland

Cyphioideae

Perennial (twining) herbs with tuberous roots; C subpolysymmetric, also 3:2; A basally connate, (anthers slightly coherent); pollen psilate; G semi-inferior, style bends away from median K but does not elongate after A dehiscence, style hairs with bulbous bases, pollen deposited in pollen box, stylar canal +[?], stigma with a fluid-filled terminal cavity with a lateral (terminal) pore; embryology?; fruit septi- and loculicidal [valves bifid]; n = 9.

1/65. Africa, esp. the south (map: from Thulin 1978, N. B., not known from Cape Verde Islands).

Sympetaly in Cyphioideae is early. For information on secondary pollen presentation, see Leins and Erbar (2003a, 2005).

Synonymy: Cyphiaceae A. de Candolle

Evolution. Divergence & Distribution. Knox et al. (2006, no Nemocladoideae or Cyphocarpoideae included) suggested that [Cyphia + Lobelioideae] originated in southern Africa, dispersing quite widely, and with at least two returns to Africa; Antonelli (2009) also suggested that Lobelioideae originated in Africa, and with much subsequent long distance dispersal of the tiny seeds.

There has been extensive diversification in the Siphocampylus-Burmeisteria-Centropogon-Lysipomia clade in South America, particularly along the Andes, and the last genus includes ca 40 rosulate species growing in the páramo (West " Ayers 2006; Sklenár et al. 2011; see also Knox et al. 2008; Antonelli 2008). The pachycaul giant lobelias are derived from herbaceous ancestors (Knox et al. 1993), and giant lobelias from widely separated parts of the globe (Pacific, South America, Africa) may be in the same immediate clade (Antonelli 2009), indeed, some South American taxa may be derived from within the African giant lobelia clade, although the relationships of the giant lobelias and the biogeographic implications of these relationships need more detailed study. Long distance dispersal is also implicated in the occurrence of Lobelia loochooensis in the Ryukus; it probably came from Australia ca 7,000 km distant (Kokubugata et al. 2012).

Givnish et al. (2006a, 2009a; see also Buss et al. 2001 - seed morphology) note that the some 130 species of Hawaiian Lobelioideae appear to have evolved from a single woody ancestor a mere ca 13 m.y.a. (ages in Antonelli 2009 are slightly older); these ages are older than that of the oldest island, but presumably there was movement from islands that subsequently have sunk. Hawaiian Lobelioideae represent a major plant radiation on the islands. Species there have a variety of growth habits and leaf morphologies, and some species are spiny; herbivory by the now-extinct moa-nalo, a flightless duck as large as a small turkey, is suspected as driving some of this variation. Fleshy fruits have evolved more than once in Hawaii, and pollinators and fruit dispersers also vary considerably (Carlquist 1970; Givnish et al. 1995).

Diversification within Campanuloideae may have begun (41-)37.4-23.5(-3.2) m.y.a. (Roquet et al. 2009, also ages for other clades, ages in different analyses varied considerably for deeper nodes). Another possible age for stem Campanuloideae is ca 41 m.y., crown diversification beginning much later, only 26.3-15.8 m.y.a. (Wikström et al. 2001). The biogeographic history of this subfamily is complex and involves much movement, the area from the Balkans to western Asia being particularly critical in its diversification (Roquet et al. 2009 for details); there are over 100 species of Campanula in Turkey alone. Within Campanuloideae there are several remarkable distribution patterms, although sampling needs to be improved; are Wahlenbergia linifolia (St Helena) and W. berteroi (Juan Fernandez sister taxa (Haberle et al. 2009)? Interestingly, Campanuloideae on Crete seem to be largely remnants of a flora that was on the island when it was originally isolated (Cellinese et al. 2009). Crown Wahlenbergia is (45.3-)29.6(-15.2) m.y. old, stem Wahlenbergia is ca 32 m.y. old (HPD: Prebble 2011); there was little diversification for ca 10 m.y., and W. krebsii, from the Cape, is sister to the rest of the genus.

Pollination Biology. For the evolution of the secondary pollen presentation devices in the family, see Erbar and Leins (1988b) and Leins and Erbar (especially 2003b, 2006, 2010). However, sampling (inc. Nemocladoideae, some Lobelioideae) is still incomplete, and understanding the evolution of these devices awaits a better supported phylogeny (see below). The flowers are initially polysymmetric in bud, they are protandrous and the introrse anthers are more or less connivent when they dehisce (e.g. Leins & Erbar 2003b, 2010). Campanuloideae have brush pollination devices, and here the pollen is caught in a brush of hairs on the style, whence they are removed by the pollinator; in the female phase, the hairs retract so any grains present fall off and selfing is prevented. However, in Pteromarula the stigmatic head is swollen and hairs occur only there (Igersheim 1993), but otherwise pollination is similar. Phyteuma has coherent corolla lobes although the corolla is open laterally; the style hairs are only partly retractile. In Lobelioideae the pollen is retained in a tube formed by the connate anthers; it is forced out by the stigma before the stigmatic lobes separate, recurve, and become receptive.

In Campanuloideae insect pollination is prevalent, but bird (and lizard) pollination is also known there, especially in taxa that grow on islands (Olesen et al. 2012). High-altitude species of Burmeistera (Lobelioideae) have both bird and bat pollination (Muchhala 2006); the latter species show character displacement, sympatric taxa differing more in floral morphology than would be expected, so reducing the chances of pollen being deposited on the wrong stigma (Muchhala & Potts 2007). In Centropogon nigricans there seems to have been co-evolution with a remarkably long-tongued bat, Anoura fistulata (Muchhala & Thomson 2009: c.f. Angraecum - Orchidaceae); all told some 110 species of Andean Lobelioideae may be bat pollinated (Dobat & Peikert-Holle 1985). Stein (1992) discusses the extrafloral nectaries of Andean Centropogon that are found on the outside of the inferior ovary, although mostly in species growing at lower altitudes, where ants are also found; in species at higher altitudes such nectaries were rare and pollination was by sickle-bill humming birds (Eutoxeres: Heliconia [Heliconiaceae] is the nectar resource for Eutoxeres at lower altitudes). Lobelioideae radiated extensively on Hawaii, and the flowers of many species of Cyanea and Clermontia (which separated from each other ca 9.7 m.y.a.) are conspicuously curved; pollination of around 125 species on the archipelago is/was by a few species of birds of the extinct and extant Drepanidae and extinct Mohoidae (Carlquist 1970; Lammers & Freeman 1986; Givnish et al. 1995; Pender et al. 2014; T. J. Givnish pers. comm. x.2013). Some species of Clemontia have petaloid sepals, a feature that may have been lost twice (Givnish et al. 2013)

The nectar of some Campanuloideae may be brightly colored and then the filament bases are not persistent; normally they are, and then they enclose the nectar.

Genes & Genomes. For the very extensive rearrangements in the chloroplast genome, including the inverted repeat, see Cosner et al. (1997, 2004), Knox and Palmer (1999: Cyphocarpus, Nemacladus, etc., not studied, Cyphia was), and Haberle et al. (2008a). The chloroplast gene accD (= ORF512, zpfA) has been lost (Doyle et al. 1995 and references) in at least some Campanulaceae. Biparental transmission of plastids has been recorded (Corriveau & Coleman 1988).

Chemistry, Morphology, etc. Since the pedicel of Lobelia and its relatives is twisted (resupinate), the flowers appears to have a "normal" orientation with the median petal abaxial, however, this does not usually occur in Lysiopoma (= pseudo-resupinate - Ayers 1997). Nemacladus (Nemacladoideae) has groups of remarkable almost hand-like (in some S.E.M.s) pseudonectaries at the bases of two adaxial filaments. It is not known if the style hairs there are retractile. In Ostrowskia (Campanuloideae) the anther has a placentoid and the integument is massive (Kamelina & Zhinkina 1998). Some species of Wahlenbergia have an almost superior ovary.

For stem-node anatomy of Campanuloideae, see Col (1904), for flowers of Downingia, see Kaplan (1969 and references), for morphology, see Shulkina et al. (2003), for fruit morphology, see Kolakovsky (1985). Further general information on the subfamilies was taken from Schönland (1889), Wimmer (1968) and Lammers (1998 and especially 2006); for pollen see Dunbar (1975a, b), Eddie et al. (2010) and Hong and Pan (2012), for embryology, etc., see Kausik and Subramanyam (1945, 1947), Rosén (1932, 1949) and Subramanyam (1949, 1970) for possibly taxonomically interesting differences in cell number of chalazal endosperm haustorium, see Murata (1995) and Buss et al. (2001) and Cupido et al. (2011 and references) for seed coat anatomy/morphology, and Shamrov and Zhinkina (1994) and Shamrov (1998) for ovules; for the protein bodies in the nuclei, see Bigazzi (1986) and Haberle (1998), and for the remarkable Nemacladus, see Morin and Ayers (2011).

Other variation that needs to be incorporated into this schema includes inflorescence type, whether basically determinate (e.g. Campanuloideae) or indeterminate (e.g. Lobelioideae). Also, details of the major variation patterns in secondary metabolites within the clade need to be established.

Phylogeny. The major groupings above are only tentative. Both the monophyly and the relationships of the poorly known Cyphiaceae (there are three subgroups) have been unclear (Lammers 1992), although they are certainly to be included within a monophyletic Campanulaceae s. l. (see Cosner et al. 1994; Gustafsson & Bremer 1995; Gustafsson 1996b; Gustafsson et al. 1996). ITS sequence data suggest that Cyphocarpus is a member of Lobelioideae (Haberle 1998, Ayers & Haberle 1999) - see also pollen (Dunbar 1975b), but if so, it has several characters in common (parallelisms?) with the Campanuloideae + Nemacladoideae clade. Furthermore, the tree presented by Haberle (1998) suggests the groupings [[Nemacladoideae + Campanuloideae] [Cyphioideae + Lobelioideae]], which, if supported by other data, may in turn imply that the polysymmetric flower of Campanuloideae with the median sepal adaxial (the "normal" condition) is a reversal from a monosymmetric flower with the median sepal abaxial. Lundberg and Bremer (2003) found what was basically a trichotomy of Cyphia, Lobelioideae, and Campanuloideae. Finally, Tank and Donoghue (2010) suggest that Cyphia is sister to Campanuloideae and Pseudonemacladus to Lobelioideae.

General relationships within Campanuloideae are discussed by Eddie et al. (2002, 2003), Cosner et al. (2004) and Olesen et al. (2012). The Campanula clade can be divided into two main clades. One of these is centred on Campanula s. str. and Rapunculus, successively sister to these are the Jasione and Musschia clades (the latter includes some species of Campanula). Wahlenbergia and other genera are interspersed in another clade, within which a few well-supported clades are becoming evident (Cupido et al. 2013). Both Campanula and especially Wahlenbergia are polyphyletic, and within the latter, W. hederacea (now = Hesperocodon hedreacea), is widely separate from the rest, linking rather with Jasione (Haberle et al. 2008b, 2009; Cellinese et al. 2009; Roquet et al. 2008, 2009; Borsch et al. 2009; Prebble et al. 2010; Cupido et al. 2013). Platycodon, Codonopsis and Cyananthus form a clade and are strongly supported as being sister to the rest of the subfamily (e.g. Cosner et al. 2004).

Within Lobelioideae, molecular data suggest that Lobelia itself is wildly paraphyletic (Knox & Muasya 2001; Antonelli 2008, 2009; Knox et al. 2008). Within South American lobelioids, Centropogon and Siphonocampylus, for example, are not monophyletic (e.g. Lagomarsino et al. 2011), but there is little support for relationships in general.

Classification. A.P.G. II (2003) suggested as an option keeping Lobeliaceae separate from Campanulaceae, but the two are best combined in view of their substantial similarities (see A.P.G. III 2009). For a world checklist and bibliography, see Lammers (2007), while Lammers (2011) provided a sectional classification for Lobelia in its current circumscription.

Generic limits need much attention, with a much more broadly delimited Campanula being a reasonable solution to its extensive paraphyly, its segregate genera being based on floral features which are unreliable guides to broad relationships (Haberle et al. 2008b; Roquet et al. 2008). Cupido et al. (2013) outline possible taxonomic solutions to the developing patterns of relationships centred on Wahlenbergia, while Hong and Pan (2012) suggested the generic pulverization of the Codonopsis area. The current classification is no better a reflection of relationships in Lobelioideae, and considerable expansion of Lobelia may be a course to take.

Previous Relationships. Takhtajan (1997) divided Campanulaceae s.l. into four families; these, plus Pentaphragmataceae and Sphenocleaceae (for the latter, see Solanales here), made up his Campanulanae. Cronquist (1989) had taken the opposite tack, recognizing a broadly circumscribed Campanulaceae, and including the other two families, plus some other families in Asterales here, in his Campanulales.

[Pentaphragmataceae [[Alseuosmiaceae [Phellinaceae + Argophyllaceae]] [Stylidiaceae [Menyanthaceae [Goodeniaceae [Calyceraceae + Asteraceae]]]]]]: corolla lobes with marginal wings [could go here].

PENTAPHRAGMATACEAE J. Agardh, nom. cons.   Back to Asterales

Pentaphragmataceae

Rather fleshy herbs, rooting at base of stem; chemistry?; cork?; wood rayless; nodes ?; hairs with uniseriate branches; leaves two-ranked, lamina usu. asymmetric, margins ± serrate (entire); inflorescences cymose, usu. scorpioid; hypanthium +; K petal-like, 2 large + 3 small, C ± deeply lobed (free), with marginal wings; stamens adnate to corolla, anthers extrorse, basifixed; pollen 2-celled, oblate, grains 3-lobed, apertures between lobes, ektexine smooth, endexine lamellate only by apertures; antesepalous septae connecting ovary with hypanthium, cavities so formed necariferous; G [2-3], style short, stigma capitate; integument ca 3 cells across; embryo sac protruding from micropyle; fruit baccate, K and C persisting; seeds minute, exotestal cells cuboid, inner walls lignified; chalazal haustorium 0, endosperm starchy; n = 54-56.

1[list]/30. South East Asia to Malesia, esp. W. Malesia (map: from Airy Shaw 1954). [Photo - Flower.]

Chemistry, Morphology, etc. The family is very poorly known. The micropylar haustorium is single-celled and the embryo is about a third the length of the seed (Kapil & Vijayaraghavan 1965).

For pollen, see Dunbar (1978), for wood anatomy, see Carlquist (1997b), for the flower, see Vogel (1998b), and for general information, see Lammers (2006).

[[Alseuosmiaceae [Phellinaceae + Argophyllaceae]] [Stylidiaceae [Menyanthaceae [Goodeniaceae [Calyceraceae + Asteraceae]]]]]: ?

Age. Estimates of the age of this node (but note topology) are (79-)73, 67(-58) m.y. (Bell et al. 2010) and (88-)84, 76(-72) m.y. (Wikström et al. 2001).

[Alseuosmiaceae [Phellinaceae + Argophyllaceae]]: plant woody; lamina gland-toothed; x = 8.

Age. An estimate of the age of this node (note topology again!) is (71-)61, 56(-44) m.y. (Bell et al. 2010) or (73-)69, 66(-62) m.y. (Wikström et al. 2001).

Phylogeny. There is a possible grouping [Alseuosmiaceae [Phellinaceae + Argophyllaceae]] or [Alseuosmiaceae [Stylidiaceae [Phellinaceae + Argophyllaceae]]] (e.g. Kårehed et al. 2000; Lundberg & Bremer 2001 respectively), and although jacknife support for the position of Alseuosmiaceae is not very strong, the posterior probability for the first grouping is 1.0 (Kårehed 2002a).

ALSEUOSMIACEAE Airy Shaw   Back to Asterales

Alseuosmiaceae

± Woody; condensed and ellagitannins +, inulin?, iridoids 0; young stem with separate bundles; true tracheids +; wood rayless, or raye narrow or broad; starch-storing living fibres +; axial parenchyma 0 (+); pericyclic fibres weakly developed; petiole bundle(s) arcuate; endodermis in both stem and leaf; hairs axillary, uniseriate; lamina vernation conduplicate, margins serrate; flowers (4-)5(-7)-merous; (hypanthium present), K free, valvate, C margins with wings, (fringed; erose; hardly - Platyspermation); stamens adnate to corolla, anthers ± basifixed; pollen (in tetrads); G [2, 3], nectary +, stigma barely expanded; ovules 2 or more/carpel; fruit baccate, calyx usually persistent; exotesta little thickened, lignified, mesotesta persistent; ?haustoria; n = 9 [Alseuosmia].

4[list]/10: Alseuosmia (5). New Guinea, E. Australia, New Zealand, New Caledonia (map: from van Balgooy 1993).

Evolution. Plant-Animal Interactions. Platyspermation and other Alseuosmiaceae on New Caledonia commonly have galled fruits or flowers.

Chemistry, Morphology, etc. Ellagitannins are reported from Alseuosmia (Kårehed 2006 for references); this should be checked. Most Alseuosmiaceae have rayless wood, living mature fibres with stored starch (Dickison 1986b), and stem with an endodermis. Uniseriate hairs in Platyspermation are not restricted to the leaf axils, although they are particularly dense there, rather, they cover the whole plant. Their persistent, reddish bases look rather like glands, hence perhaps the past inclusion of the genus in Rutaceae...

There are tanniniferous cells in the flower. The margins of the corolla lobes of Platyspermation have narrow flanges and papillae; the corolla is only shortly tubular, the lobes being rather spreading (buzz pollination?). The pollen of Alseuosmia linariifolia is described as being tricolpate, with an ectexine made up of a thick, tubercular tectum and massive, spherical columellae (Polevova 2006); whether this can be generalised to the family is unclear (see also Kårehed 2006).

Some details of vegetative anatomy are taken from Paliwal and Srivastava (1969), Dickison (1989a) and Gornall et al. (1998), and of testa anatomy from Nemirovich-Danchencko and Lobova (1998) and Takhtajan (2000). The embryology is poorly known. See Kårehed (2006) for general information.

Phylogeny. Platyspermation is strongly associated with other Alseuosmiaceae (Lundberg & Bremer 2001), and may be sister to the rest of the family (Tank & Donoghue 2010).

Classification. Generic limits are in some dispute (Tirel 1996).

Previous Relationships. Genera now included in Alseuosmiaceae have previously been placed in Caprifoliaceae, Rubiaceae, Rutaceae, Ericaceae, Epacridaceae, etc. Although the family was recognized by Takhtajan (1997), it was included in his Hydrangeales.

Synonymy: Platyspermataceae Doweld

[Phellinaceae + Argophyllaceae]: cork subepidermal; pollen (spiny), with rugulose exine; style short; ovules apotropous.

Age. Estimates of the age of divergence of this family pair are (68-)63, 62(-57) m.y. (Wikström et al. 2001).

PHELLINACEAE Takhtajan   Back to Asterales

Phellinaceae

Trees; benzylisoquinoline alkaloids + [homoerythrina], inulin, iridoids?; true tracheids +; rays very broad [to 14 cells across]; sclerenchyma surrounding leaf veins; petiole bundles annular; cuticle waxes as platelets and rodlets; lamina margins serrate (entire); plant dioecious, flowers small, 4-6-merous; K connate basally, ± open, C free; nectary 0?; staminate flowers: filaments shorter than the anthers; pistillode +; carpellate flowers: staminodes +; G superior, [2-5], style ± 0, stigmas large, lobed; ovule 1/carpel, apical; fruit a drupe, stones separate; testa ?; endosperm haustoria?; n = 17.

1[list]/12. New Caledonia.

Chemistry, Morphology, etc. The guard cells are huge, with inner and outer stomatal ledges. The ovules are reported as being hemitropous to campylotropous, but Phelline is embryologically poorly known.

See Baas (1975) for wood anatomy (it appeared to be extremely primitive), Lobreau-Callen (1977) for pollen, and Kårehed et al. (2000) and Barriera et al. (2006) for much additional information.

Previous Relationships. Takhtajan (1997) placed the family in Icacinales, describing the leaves as being mostly estipulate, while Cronquist (1981) placed it in his Aquifoliaceae (adjacent to Icacinaceae - both in Celastrales).

ARGOPHYLLACEAE Takhtajan   Back to Asterales

Argophyllaceae

Shrubs; gallic acid +, inulin?; (nodes 1:1, 5:5); petiole bundles arcuate; hairs T-shaped, multicellular, with slits over the stalk cell; lamina vernation supervolute-curved [Corokia macrocarpa], margins entire; flowers 4-5(-8)-merous; K valvate [always?], C basally connate, with adaxial fringed ligule, (and marginal wings); G (1) [2, 3(-5)], (semisuperior), nectary + [Corokia], stigma punctate, lobed, or capitate, wet; ovule 1 or several/carpel, apical, apotropous, integument 6-7 cells across, nucellus base massive; fruit a septicidal + septifragal capsule [Argophyllum] or drupe [Corokia]; exotestal cells with inner walls massively thickened and lignified [Argophyllum] or all walls somewhat thickened [Corokia]; endosperm hemicellulosic, (embryo medium); n = 9.

2[list]/21: Argophyllum (15). S.W. Pacific, including Rapa (map: from van Steenis & van Balgooy 1966). [Photo - Corokia Flower © Gardenweek.org.]

Chemistry, Morphology, etc. Septate fibres and vascular tracheids are present (Patel 1973; Noshiro & Baas 1998), but the significance of this is unclear. The guard cells in Argophyllaceae are raised above the epidermis (Kårehed et al. 2000). There are tanniniferous cells in the flower, as in Alseuosmiaceae. The pollen is like that of Cornaceae, with complex H-shaped endoapertures (Ferguson 1977).

See also Eyde (1966) and Kårehed (2006) for general information, Mauritzon (1933) for a little embryology, Lobova (1997) for testa, and Gornall et al. (1998) for vegetative anatomy.

Previous Relationships. Along with Cornaceae, Argophyllaceae were placed in Hydrangeales by Takhtajan (1997), while Cronquist (1981) included them in his very heterogeneous Grossulariaceae.

Synonymy: Corokiaceae Takhtajan

[Stylidiaceae [Menyanthaceae [Goodeniaceae [Calyceraceae + Asteraceae]]]]: inulin +.

STYLIDIACEAE R. Brown, nom. cons.   Back to Asterales

Young stem with separate bundles; nodes 1:1; lamin margins entire, petiole 0; C imbricate; nectary +; A 2, anthers extrorse; pollen colpate; integument 4-6 cells across; synergid cells elongated; micropylar and chalazal endosperm haustoria +; embryo "minute".

3[list]/245 - 2 subfamilies below. Scattered in South East Asia to New Zealand, S. South America, but mostly Australia.

Age. An estimate of the age of crown-group Stylidiaceae is (80-)71, 65(-57) m.y. (Bell et al. 2010), and another is (78-)73, 70(-65) m.y. (Wikström et al. 2001).

Donatioideae

1. Donatioideae B. Chandler

Dwarf cushion herbs; iridoids?, tanniniferous; cork cortical?; mucilage cells +; stomata also paracytic; hairs uniseriate, axillary; flowers solitary, terminal; K 3-7, free, C 5-10, free; A also 3, free; nectary annular; pollen nuclei?; G [2-3], styles separate, somewhat recurved, stigmas capitate; hypostase +; fruit indehiscent; seed coat?; embryo suspensor short; n = 24.

1/2. New Zealand, Tasmania, S. South America. [Photo - Habit, Flower © Univ. of Tasmania.]

Synonymy: Donatiaceae B. Chandler, nom. cons.

2. Stylidioideae Kittel

Stylidioideae

Herbs (climbers), cushion plants; cork also outer cortical; vascular bundles closed, scattered or in a single ring; cambium develops just inside the endodermis, storied, secondary tissue developing towards the inside only, xylem with intra/interxylary phloem; vessel elements with simple perforation plates; hairs glandular; leaves pseudoverticillate or in rosettes, with axillary hairs; flowers with the odd sepal adaxial, often semi-resupinate, (split-monosymmetric); K connate, (6), C connate, 4 in two pairs, or 4 + labellum, early tube formation, often with coronal appendages, (spurred), or 5-6(-9); nectary as paired ad-/abaxial lobes (1 lobe); A completely adnate to style [= gynostemium], anther thecae set end to end, (apically connate); pollen grains prolate [?level], (3 nucleate), 3-8-colpate; G [2] (adaxial much reduced), placentation free-central, stigma small, dry; fruit capsular, septicidal (indehiscent); seed exo-endotestal, exotestal cells sclerosed; embryo often with single cotyledon; n = 5-16, protein bodies in nucleus.

2(-5)/240: Stylidium (220-300). Mostly Australia, especially Western Australia, scattered in the central part, also Sri Lanka to South East Asia, Malesia, New Zealand, and S. South America (map: see Erickson 1958; Australia's Virtual Herbarium xi.2012). [Photo - Flower.]

Evolution. Divergence & Distribution. Diversification in Stylidioideae has been dated to ca 39 m.y.a. (Wagstaff & Wege 2002).

Pollination Biology. In many Stylidioideae (Stylidium s.l.) the two stamens are adnate to the style, the extrorse anthers being borne near the stigma. The whole complex (a gynostemium), sometimes called a column, is often sensitive, moving rapidly when brushed by pollinator; in some species the column is hinged. For the literature on stylar movement, see Findlay and Findlay (1989). In Levenhookia, however, the gynostemium is held under tension in the hooded labellum, flipping only when the latter is disturbed. Armbruster et al. (1994) found that species of Stylidium in the Perth area were pollinated mostly by solitary bees and bombyliid flies, species in the same locality differing both in corolla tube and in column lengths; even the pollen varied in colour.

Ecology & Physiology. There are suggestions that Stylidium may be carnivorous. Insects are trapped by the glandular hairs, which also show yeast-extract stimulated protease acivity; the plants grow in acid, nutrient-poor soil like other carnivorous plants. However, uptake of nutrients by the plant from the insects has yet to be demonstrated (Darnowski et al. 2006).

Chemistry, Morphology, etc. In Stylidioideae the cambium may develop beneath the endodermis; xylem, and sometimes also phloem, is produced towards the inside, and at most cork to the outside (Carlquist 1981a). In older stems of Donatia the cortex is very thick, and the vascular tissue forms a narrow cylinder in the center (Chandler 1911).

Carolin (1960b) drew the anthers of Donatia as being introrse. The fertile stamens are the adaxial pair. Ronse de Craene (2010) described the flower of Stylidium graminifolium as being obliquely monosymmetric at maturity, and the corolla and parts inside are illustrated as having rotated ca 60o relative to the calyx, and there is only a single abaxial (in the text described as being adaxial) nectary. See also Erbar (1992) for floral development, which needs more study in the family as a whole. The pollen of at least some Stylidiaceae has a very distinctive inner ectexine that lacks columellae but is permeated by numerous sinuous channels (Polevova 2006). Monocotyly is reported to be quite common in Stylidioideae, at least (Carlquist 1981b).

For anatomical differences between Donatioideae and Stylidioideae, see Repson (1953). The proembryo in Donatia is ovate, the suspensor is made up of short cells, but in Stylidioideae it is long, and is made up of cells that are longer than broad (Philipson & Philipson 1973), as in other Asterales (Tobe & Morin 1997). The leaves of Donatia are very small, and their venation is acrodromous.

For general information, see Carolin (2006), Carlquist and Lowrie (1989: Stylidioideae), Australian Plants 27(215). 2013, and Glenny (2009: Forstera); some anatomical details can be found in Thouvenin (1890), for embryology, see Rosén (1935) and Subramanyam (1951a), for placentation, see Carolin (1960a), for protein bodies, see Thaler (1966), and for the testa anatomy of Stylidium, see Tobe and Morin (1996).

Phylogeny. Donatia is clearly sister to the rest of the family, but there is some uncertainty over further relationships. Laurent et al. (1999) found that Forstera s.l. was sister to the rest of the family in combined molecular and morphological analyses, but the topology had litle support, in a rbcL + ndhF analysis it was grouped with Levenhookia, but with only weak support; Wagstaff and Wege retrieved the former topology in an analysis based on variation in ITS and rbcL. In gross floral morphology Donatia and Forstera are similar, both having basically radially symmetrical flowers that are whitish in colour.

Previous Relationships. Stylidiaceae have been treated as two families in Stylidiales (Takhtajan 1997) or merged in one family (Philipson & Philipson 1973). A.P.G. II suggested as an option keeping Donatiaceae and Stylidiaceae separate, although the two can reasonably be combined (e.g. Lundberg & Bremer 2003; A.P.G. III 2009).

[Menyanthaceae [Goodeniaceae [Calyceraceae + Asteraceae]]]: caffeic acid +; vessel elements with simple perforation plates; inflorescence with a terminal flower, single flowers and then cymes below; C connate, early tube formation, with strong ± fused marginal [commissural] veins joining the median near the apex; stamens adnate to corolla; tapetal cells bi- or multinucleate; pollen more or less psilate; G [2]; integument >10 cells thick, antiraphal vascular bundle proceeding to the micropyle; endosperm haustoria 0, embryo long; x = 9.

Age. One estimate of the age of this node is (71-)63, 58(-48) m.y. (Bell et al. 2010), and another is (73-)69, 65(-61) m.y. (Wikström et al. 2001).

Evolution. Divergence & Distribution. Pollen of all families of this clade - and of some subfamilies of Asteraceae - had differentiated by the Oligocene, and has been found in many places that are fragments of the Gondwanan continent (Barreda et al. 2010a).

Presence of sclereids, binucleate pollen, and multi-nucleate tapetal cells may also be synapomorphies for this clade (Lundberg 2009, q.v. for more possible synapomorphies).

Chemistry, Morphology, etc. The androecium has spiral initiation in some Menyanthaceae, Asteraceae and Goodeniaceae - and also Araliaceae (Erbar 1997). For other characters common to this clade, see Anderberg et al. (2006, c.f. vessel perforation plates). Vegetatively and florally Menyanthaceae are rather different from many other Asterales, however, both Menyanthaceae and Goodeniaceae have corolla lobes with marginal wings, here placed as apomorphies for both groups (or they could be a synapomorphy for the whole clade, being lost later). For inflorescence morphology and evolution, see Pozner et al. (2012).

Previous Relationships. Menyanthaceae do not link with the other three families in the four-gene study of Albach et al. (2001b).

MENYANTHACEAE Dumortier, nom. cons.   Back to Asterales

Menyanthaceae

Aquatic or marsh herbs; flavonols only +, little oxalate accumulation, tannin 0; cork?; vascular cambium 0[?]; vascular bundles separate, often scattered; nodes also 5:5; intercellular canals +; branched sclereids +; petiole bundles arcuate to annular or scattered; leaves also two-ranked, (palmately compound), lamina vernation involute, secondary veins palmate, margins usu. with hydathodal glands, crenate, colleters +, leaf base broad, petiole margins ± winged; flowers heterostylous (not); K basally connate, C lobes with marginal wings and/or with (marginal) fimbriae; ("staminodes" +, fringed and scale-like); anthers sagittate; tapetal cells with fused nuclei; pollen (two-celled), colpate; nectary +; G ± superior, placentation parietal, (style 0), stigma bilobed-spathulate, wet; fuicle vasclarized, integument 3-11 cells across; fruit a (septi- and) loculicidal capsule, (berry - Liparophyllum); seeds many, (hairy; carunculate), exotestal cells with outer walls thickened, often with a variety of projections, (meso- and endotestal cells sclerotic); endosperm oily; n = (17), protein bodies in nuclei; rpl2 intron missing.

5[list]/ca 58: Nymphoides (40). World-wide (map: from Heywood 1978, modified by Hultén 1971; Australia's Virtual Herbarium xii.2012). [Photo - Flower, Collection, Flower.]

Age. An estimate of the age of crown-group Menyanthaceae is (58-)54, 51(-47) m.y. (Wikström et al. 2001) and another is (60-)47, 44(-31) m.y. (Bell et al. 2010).

For fossil pollen, see Barreda et al. (2010a).

Evolution. Divergence & Distribution. Has the superior ovary of Menyanthaceae with its parietal placentation been derived from a more or less inferior ovary with axile placentation (c.f. Pittosporaceae - Apiales)?

Chemistry, Morphology, etc. Kasinathan and Kumari (2001) thought that the leaves of Nymphoides were opposite, indeed, plant architecture in that genus is complex (Richards et al. 2010). The vascular anatomy of the flower implies a basic monosymmetry - the lateral corolla traces are fused (Wood & Weaver 1982). There are sometimes fringed scales, "staminodes", on the corolla tube alternating with the stamens. Johri et al. (1992) suggested that the endosperm stores starch.

For embryology, see Stolt (1921) and Maheswari Devi (1963), for seed morphology, see Chuang and Ornduff (1992), for floral development, see Erbar (1997), for the missing rpl2 intron, see Downie et al. (1991b), and for general information, see G. Kadereit (2006).

Phylogeny. Relationships within Menyanthaceae have been clarified by Tippery et al. (2006, 2008) and Tippery and Les (2008); [Menyanthes + Nephrophyllidium] are sister to the rest of the family while Villarsia is very much paraphyletic. Many relationships within Nymhoides are as yet poorly supported; whether or not the flowers are heterostylous seems evolutionarily very labile (Tippery & Les 2011).

Previous Relationships. The iridoids of Menyanthaceae differ chemically from those of Gentianaceae, in which Menyanthaceae used to be included, although placentation, etc., are similar. Menyanthaceae were placed in Solanales by Cronquist (1981), but inulin storage i.a. is inconsistent with that position. Branched sclereids and air canals are similarities between Menyanthaceae and Nymphaeaceae, but both are aquatics.

[Goodeniaceae [Calyceraceae + Asteraceae]]: acetylenes +; secondary pollen presentation + [flowers protandrous, anthers connivent at dehiscence, style elongates after pollen deposition]; pollen with bifurcating columellae; stigma dry, ± papillate; K persistent in fruit.

Age. Kim et al. (2005) date this node to (80-)64.5(-49) m.y.a., Wikström et al. (2001: c.f. topology) to (43-)50, 44(-41) m.y., Naumann et al. (2013) to 52.4 m.y., Bell et al. (2010: also c.f. topology) to only (50-)44, 40(-30) m.y., and Xue et al. (2012) to 39.7-39.0 m.y. - still going down.

Chemistry, Morphology, etc. There is considerable variation in details of pollen presentation in this clade (Leins & Erbar 2003b, 2006 and references). Study of early capitulum development in Arnaldoa macbrideana (Asteraceae - Barnadesioideae) suggests that the capitulum there is built up of partial inflorescences with cymose branching, so perhaps linking the racemose heads of Asteraceae with the apparently rather different inflorescences of many Calyceraceae and Goodeniaceae (Leins & Erbar 2003b, see their polytelic thyrses). Acicarpha is the only Calyceraceae with n = 8, and it is also the only member of that family with a possibly plesiomorphic condensed spicate inflorescence (DeVore 1994). For a comparison of the pollen of the three families, see DeVore et al. (2007), for chromosome numbers see Semple and Watanabe (2009).

Phylogeny. Leins and Erbar (2003b) concluded that Goodeniaceae are probably sister to Asteraceae, noting i.a. that Barnadesia polyacantha has a bulge beneath the style branch, perhaps homologous with the stylar cup of Goodeniaceae. Soltis et al. (2007a) found the relationships [Asteraceae [Calyceraceae + Goodeniaceae]].

GOODENIACEAE R. Brown, nom. cons.   Back to Asterales

All except Scaevola

Herbs (woody, arborescent); O-methyl flavonols only, alkaloids, polyacetylenes +; cork also cortical; (vessel elements with scalariform perforation plates); (medullary vascular bundles +); nodes 1:1 (3:3, 5:5 - cortical bundles = leaf traces); branched sclereids +; indumentum variable, hairs often minutely warty; lamina margins entire to toothed; flowers split-monosymmetric; C induplicate-valvate, (spurred), lobes with marginal wings; A basifixed; pollen binucleate, mesocolpia concave; nectary usu. 0; G also [4] ([2]), (placentation ± basal), style with apical hairy pollen-collecting indusium and stylar cup, curved, stigma bilobed; ovules 1 or more/carpel, integument 6-20 cells across, hypostase +; synergids long, hooked, antipodal cells persistent; fruit dehiscing laterally, septicidal (and loculicidal) (drupe, nut); testa 7-14 cells thick, exotestal cells usu. palisade (crystalliferous), all walls (especially inner) thickened, (hypodermal layers lignified); n = 9; rpl16 intron missing.

12[list]/430. Very largely Australian, Scaevola alone pantropical (map: esp. Leenhouts 1957b, excluding Scaevola).

1. Dampiera, etc.

Anthers connate; stigma not protruding past the indusium.

3/97: Dampiera (66). Australia (S. New Guinea).

[Brunonieae + Goodenieae]: pollen microspinulose, columellae branching, stigma protruding past the indusium.

2. Brunonieae G. Don

Herbs; inflorescence capitate, involucrate; K with filamentous hairs, C polysymmetric, lobes lacking marginal wings; G superior; ovule 1/carpel; testa thin-walled, compressed; endosperm 0.

1/1: Brunonia australis. Throughout Australia.

Synonymy: Brunoniaceae Dumortier, nom. cons.

3. Goodenieae Dumortier

Scaevola

Herbs to shrubs; (C lobes lacking marginal wings); A adnate to base of C; n = 8 (7).

Ca 8/330: Goodenia (190), Scaevola (100). Throughout Australia, to New Zealand, Chile and China; Scaevola pantropical, with the coastal S. taccada in the E. and C. Pacific and Indian Oceans and S. plumieri in the W. Indian, E. Pacific and the Atlantic oceans (from van Balgooy 1975). [Photo - Flower.]

Synonymy: Scaevolaceae Lindley

Evolution. Divergence & Distribution. For fossil pollen, see Barreda et al. (2010a). Some diversification in Scaevola may be associated with the aridification of the Nullarbor Plain some 14-13 m.y.a. separating eastern and western clades (Crisp & Cook 2007).

Pollination Biology & Seed Dispersal. For the diversity of pollen presentation devices in the family, see Erbar and Leins (1988) and Leins and Erbar (2003b, 2010). In nearly all species the pollen is initially enclosed by the indusium, and is pushed out by the elongating style; Brunonia, with its capitate inflorescence and flowers with straight styles, also has pollen caught in a brush formed by stylar hairs.

The seeds of many Goodeniaceae are myrmecochorous (Lengyel et al. 2009, 2010).

Chemistry, Morphology, etc. The lateral veins of the corolla of Brunonia unite in the receptacle (Erbar 1997). The pollen is distinctive; endoapertures are bordered (with orae) and lalongate and the spines are rounded (Gustaffson et al. 1997). The mitochondrial genes cox1, atp1 and matR showed massive divergence (Barkman et al. 2007: Scaevola only sampled).

See Subramanyam (1950a) for embryology, Carolin (1978, 2006) for general variation and morphology and Erbar and Leins (1988) and Cave et al. (2010) for the floral development of Brunonia.

Phylogeny. Relationships within Goodeniaceae are becoming fairly well understood (Gustafsson 1996a; Gustafsson et al. 1996; Jabaily et al. 2010, esp. 2012). There are two main clades, Leschenaultia and allies, and the other Scaevola, a paraphyletic Goodenia, and allies. Within the latter clade Brunonia is sister to the rest, and most of the numerous features in which it differs from other Goodeniaceae seem to be autapomorphies (see above). Some of these features might seem to suggest relationships with Asteraceae (Gustafsson 1996a), but clearly the exclusion of Brunonia would make Goodeniaceae paraphyletic (Jabaily et al. 2012).

Classification. For a general account of most of the family, see Fl. Austral. 35. 1992).

Thanks. I am grateful to Mats Gustafson for comments.

Synonymy: Brunoniaceae Dumortier, nom. cons., Scaevolaceae Lindley

[Calyceraceae + Asteraceae]: inflorescence capitate, involucrate; flowers small, sessile; C tubular, deeply lobed, commissural veins connate; filament collar +; pollen prolate, columellae [in endosexine] evenly spaced, pollenkitt +; ovule single [per flower]; fruit a cypsela, K persistent, modified, involved in dispersal.

Age. These two clades diverged an estimated (49-)45.5(-42) m.y.a. (K.-J. Kim et al. 2005) or ca 51 m.y.a. (Bremer et al. 2004).

Evolution. Divergence & Distribution. Both Calyceraceae and Asteraceae-Barnadesioideae, sister to the rest of Asteraceae, are South American, and this whole clade may have originated there.

For other similarities or possible synapomorphies, see DeVore (1994) and Lundberg and Bremer (2001, 2003), these include libriform fibres with simple pits and vasicentric parenchyma. Pesacreta et al. (1994) suggest similarities in the micromorphology of the filaments and connective bases between at least some members of Calyceraceae and Asteraceae.

Placement of characters like pollen with intercolpar depressions on the tree is difficult to ascertain (see also DeVore 1994; DeVore et al. 2000); DeVore and Skvarla (2008) suggest that pollen characters thought to suggest a relationship between the two families are different in detail and are therefore not homologous. Thus although both families have but a single ovule, the position and orientation of the ovule is such that the single ovule condition may well have been derived independently. Similarly, the inflorescence, although superficially similar in the two families, may be cymose in Calyceraceae and racemose in Asteraceae.

Chemistry, Morphology, etc. Calyceraceae and Barnadesioideae have a similar simple flavonoid profile. For inflorescence morphology, see Pozner et al. (2012).

Previous Relationships. Both Cronquist (1981) and Takhtajan (1997) placed the two families in separate, if adjacent, orders.

CALYCERACEAE Richard, nom. cons.   Back to Asterales

Calyceraceae

Herbs; ?flavonols 0; cork?; vascular bundles separated; nodes ?; pericyclic fibres 0; plant ± glabrous; lamina margins entire; inflorescence bracteate; flowering ± centrfogal, made up of cymose units, (not obvious, but a terminal flower - Acicarpha); K connate, aerenchymatous or spine-like, C outer layer separates and photosynthesises, midvein proceeding to apex beyond fusion with laterals; nectaries externally alternating with filaments in C/A tube, opening at apex of C/A tube; filaments ± connate, anthers basally connate, ?exodermis +; pollen binucleate, with intercolpar depressions, spinulate or not; (G embedded in inflorescence axis), stigma capitate, pollen deposited on its top; ovule apical, apotropous; apex of fruit with a conical body [persistent base of C and style]; seed coat undistinguished, chlorophyllous; endosperm +; n = 8, 12, 13, 15, 17, 18, 20-22, chromosomes small, 1.6-2.7 µm long, centromeres (sub)metacentric, mostly centromeric C-bands, interphase nucleus areticulate, chromocentres sharply differentiated.

4[list]/60: Boopis (30). South America (map: from Heywood 1978 [S. part of range]; DeVore 1994). [Photos - Acicarpha Habit, Calycera © H. Wilson., Undetermined Flowers]

Age. Acicarpha and Boopsis diverged ca 51 m.y.a. (Bremer et al. 2004).

Pollination Biology. There is secondary pollen presentation of the pump mechanism type (e.g. Erbar 1993).

Chemistry, Morphology, etc. Cronquist (1981) described the flowers as being sometimes "slightly irregular"; they are commonly polysymmetric. There may be five carpels (e.g. Erbar 1993). The integument is described as being "thick" and the outer cell layers contain chloroplasts (Dahlgren 1915).

Some general information is taken from Hansen (1992: especially useful), DeVore (1994), DeVore and Stuessy (1995), and Hellwig (2006), some details of morphology come from Pontiroli (1963), embryology from Dahlgren (1915: one species), floral development from Erbar (1993: one species, and very odd development at that), inflorescence development from Harris (1999: two species) and cytology from Benko-Iseppon and Morawetz (2000b: one species). This family needs work!

Synonymy: Boopidaceae Cassini

ASTERACEAE Berchtold & J. Presl, nom. cons.//COMPOSITAE Giseke, nom. cons. et nom. alt.   Back to Asterales

Asteraceae

Iso/chlorogenic acid, isoflavonoids, pentacyclic triterpene alcohols, terpenoid essential oils, (various alkaloids), polyacetylenes + [?level], a variety of fatty acids in the seeds, tannins, iridoids 0; vascular bundles separated (a cylinder - woody taxa); (cork deep seated); (cortical or medullary vascular bundles +); cambium storied or not; (vessel elements with scalariform or reticulate perforations); nodes also 5:5; schizogenous secretory canals +; (leaves opposite), lamina vernation often conduplicate or revolute, margins various; inflorescence lacking a terminal flower, involucral bracts in several series; receptacle scrobiculate, bracts/bracteoles 0; heads homogamous; marginal and central flowers polysymmetric; K reduced, C midveins 0 (+), (3-lobed ray corolla), lobes of disc corollas usu. longer than wide; anthers connate, with conspicuous apical appendage, basally calcarate [sagittate], caudate [theca with basal appendage], (laciniate), endothecial cells elongated parallel to main axis of anther [?level]; tapetum amoeboid (secretory); pollen 37-49.1 µm in diam., exine 6.1-6.7 µm across, tectum microperforate; nectary annular; style branched, branches [arms] rounded at apex, short [<1.4 mm long], stigmatic surface continuous on inner surfaces; ovule basal, epitropous, integument 6-20 cells across; embryo sac with elongated synergid cells, antipodal cells often persistent, proliferating and/or multinucleate; K pappose in fruit, pappus capillary; (testa not vascularized), exotestal cells thickened, palisade or flattened, or undistinguished; endosperm scanty to 0, (nuclear); protein bodies in nuclei; sporophytic incompatibility system present.

1620[list]/23,600 - twelve groups below. World-wide (map: Vester 1940; Hultén 1971). [Photo - Flowers, and more Flowers.]

Age. Crown-group Asteraceae ar dated to some 42-36 m.y. (K. J. Kim et al. 2005), (52-)43, 40(-31) m.y. (Bell et al. 2010), or (44-)41, 40(-37) m.y. (Wikström et al. 2001); other suggested ages are similar (Funk et al. 2009c for a summary; see also Torices 2010). However, Beaulieu et al. (2013a: 95% HPD) estimated a somewhat older crown-group age of (52-)49(-48) m.y. (Heads [2012] thought that the mostly Antipodean Abrotanella, basal Senecioneae, diverged from the rest of the tribe in the Jurassic or Early Cretaceous, which would thus imply an age for Asteraceae as a whole of around 1,500,000,000 years, or about a third of that age, depending on which vicariance dating you elect to pick [Swenson et al. 2012].)








Asteraceae

1. Barnadesioideae Bremer & Jansen

Barnadesioideae

Usually woody; notably poor in flavonoids, flavones 0; paired axillary thorns/spines + (0); hairs tricellular [a pedicel cell (= "golf-tee cell"), ± globose cell, and elongated cell - throughout plant]; (receptacle hairy); marginal (and central) flowers ± monosymmetric, lobing variable, (if bilabiate, 1 + 4), corolla hairy; (pollen lophate), (with intercolpar depressions), (± caveate); (style strongly curved - Fucaldea stuessyi), surface (minutely) papillate (below bifurcation), (widened at apex); achenes ?-ribbed, hairy, pappus uniseriate, villous, foxy coloured; n = 9, 25-27.

9/94. South America, esp. Andean (map: see Karis et al. 1992; Ezcurra 2002; Funk & Roque 2011). [Photo - Flower.]

[Stifftioideae, Mutisioideae [Wunderlichioideae [Gochnatioideae [Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]]]]: often herbaceous; (benzofurans + [benzene + furan - C4H40 (heterocyclic) rings]); leaves usu. triplinerved; (corolla lobing 2 + 3); (style with rigid sweeping hairs), (style arms long); achenes with twin hairs [unicellular to uniseriate base, apical cell un/equally 2-armed], pappus capillary, developing late, 2-5-seriate; 22.8 kb chloroplast DNA inversion, and 3.3 kb inversion nested within it.

Age. The age of this node is about (45-)37, 35(-27) m.y. (Bell et al. 2010), (39-)36, 34(-31) m.y. (Wikström et al. 2001), or 54.7-47.8 (Naumann et al. 2013).

2. Mutisioideae Lindley

(Receptacle hairy); (heads heterogamous), (central flowers subligulate, etc.); (corolla lobing 4 + 1); apex of anther appendage rounded (acute); styles branches variable at apex, surface papillose (below branches), (collector hairs at apex); achenes 5- or 10-ribbed, hairy to glabrous, (pappus uniseriate); n = (6-)9(+); (genome duplication).

44/630: Acourtia (65), Chaptalia (60), Mutisia (50), Trixis (50), Gerbera (35). South America.

Synonymy: Mutisiaceae Burnett, Nassauviaceae Burmeister, Perdiciaceae Link, nom. inval.

3. Stifftioideae Panero

(Marginal, central flowers ± monosymmetric); (C lobes long, ± coiled); apex of anther appendage ± acute; style surface usu. glabrous, branches ofen 1.5< mm long; achenes 10-ribbed, glabrous.

Ca 10/40. Venzuelan-Guianan (Andes, N.E. South America).

[Wunderlichioideae [Gochnatioideae [Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]]]: sesquiterpene lactones + {level?].

4. Wunderlichioideae Panero & Funk

(Receptacle alveolate), (paleaceous - Wunderlicheae); (marginal flower monosymmetric); apex of anther appendage acute to apiculate; (pollen spiny); (style and style branches surface papillose - Wunderlichieae); achenes 10-ribbed, hairy to glabrous, (pappus paleaceous); deletion in rpoB gene.

Ca 8/24. Venzuelan-Guianan (E. South America, S.W. China).

[Gochnatioideae [Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]]: ?

5. Gochnatioideae Panero & Funk

(Receptacle alveolate); (heads heterogamous); apex of anther appendage ± apiculate; pollen anthemoid[!]; style branches surface glabrous; achenes 5-ribbed, hairy, (pappus uniseriate); n = 22, 23, 27.

4 (?5)/90: Gochnatia (70). Central and South America, esp. the Caribbean and southern South America.

[Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]: pollen grains spherical [?level], columellae sausage-like; deletion in rpoB gene.

Age. The crown age of this clade is some 38-32 m.y. (K.-J. Kim et al. 2005).

6. Hecastocleidoideae Panero & Funk

Shrubby; leaves spiny; capitulae 1-flowered, grouped into synflorescence, with attractive synflorescence bracts; all flowers polysymmetric, corolla 5-lobed; apex of anther appendage rounded; pollen tricolpate; style branches surface glabrous; achenes 5-ribbed, glabrous, "pappus with scale-like corona", uniseriate; n = 8.

1/1: Hecastocleis shockleyi. S.W. U.S.A.

[Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]: (heterocyclic sulphur compounds +) [thiophene/thiofuran - C4H4S - and oligomers]; leaf triplinervation?; carpels of disc flowers [at least] superposed, sweeping hairs +[?]; achene ribbing and hariry/glabrous?; x = 10; deletion and insertion in rpoB gene.

7. Carduoideae Sweet

Plant often herbaceous, biennial habit common; (laticifers +), (resin ducts +); leaves dissected, teeth spine-tipped; flowers polysymmetric (monosymmetric); pollen (psilate), with internal tectum; ring of hairs below style branches; (achenes lacking twin hairs), (pappus uniseriate); exotestal cells palisade; n = 12.

83/2780: Centaurea (695), Cousinia (655), Saussurea (300), Cirsium (250), Jurinea (200), Echinops (120), Carduus (90), Serratula (70), Dicoma (65), Onopordum (60). World-wide, but most N. hemisphere, esp. Eurasia/N. Africa (map: from Hellwig 2004).

Age. Barres et al. (2013) estimated the age of crown Carduoideae as middle Eocene and somewhat over 40 m.y.a.; the comparable age in K.-J. Kim et al. (2005) was 29-24 m.y.a..Synonymy: Acarnaceae Link, nom. illeg., Carduaceae Berchtold & J. Presl, Carlinaceae Berchtold & J. Presl, Centaureaceae Berchtold & J. Presl, Cnicaceae Vest, Cynaraceae Burnett, Echinopaceae Berchtold & J. Presl, Serratulaceae Martynov, Xeranthemaceae Döll

[Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]: pollen with unbranched columellae.

8. Pertyoideae Panero & Funk

Herbs to shrubs; flowers not bilabiate, corolla unequally divided; (pollen with solid spines); style branches short, pilose to papillose abaxially, apices rounded (to acuminate); pappus usu. uniseriate; of (plumose) bristles; n = 12-15.

5-6/70: Ainsliaea (50). Afghanistan to East (and Southeast) Asia.

[Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]: pollen echinate.

9. Gymnarrhenoideae Panero & Funk

Plant annual, amphicarpic; heads grouped into synflorescence; anthers lacking apical appendages, ecaudate; ?pollen caveate; style branches long, ?hairs; pappus of scales; n = 9, 10.

1/1: Gymnarrhena micrantha. North Africa to the Middle East.

[Cichorioideae [Corymbioideae + Asteroideae]]: style branches medium to long [strict definition?, position on tree?]; deletion in ndhF gene.

Age. The age of this node is about (31-)28, 24(-21) m.y. (Wikström et al. 2001), (37-)29, 27(-19) m.y. (Bell et al. 2010), or 42-38.8 m.y. (Naumann et al. 2013).

10. Cichorioideae Chevallier

Plants often herbaceous, perennial; (latex + - Cichorieae); (all flowers ligulate - Lactuceae), (true ray florets +), (pollen caveate), (lophate), (with internal tectum), columellae aggregated under spines; carpels collateral, style trunk hairy, apices of style branches acute, hairs usually acute; n = (7-)9-10(-13).

224/3600: Vernonia (800-1000, but see below), Crepis (200), Scorzonera (175), Lactuca (125), Lepidaploa (115), Tragopogon (110), Lessinganthus (100), Hieracium (90-1000+: apomixis), Vernonanthura (65), Hypochaeris (60), Sonchus (60), Taraxacum (60-500+: apomixis). World-wide.

Synonymy: Aposeridaceae Rafinesque, Arctotidaceae Berchtold & J. Presl, Cichoriaceae Jussieu, nom. cons., Lactucaceae Drude, Picridaceae Martynov, Vernoniaceae Burmeister

[Corymbioideae + Asteroideae]: pollen lacking columellae in endosexine spanning space above foot layer [fully caveate], with internal foramina.

11. Corymbioideae Panero & Funk

Corymbioideae

Plant herbaceous, perennial; sesquiterpene lactones 0, macrolides +; leaves linear, with parallel veins; heads with 1 flower, involucral bracts 2; C with broad, patent lobes; anthers black; style branches long, apices variable; pappus of bristles or scales; n = 8.

1/7. South Africa (map: from Weitz 1989).

12. Asteroideae Lindley

Plants shrubby to herbaceous; sesquiterpene lactones at biogenetic levels 3 and 4 [sic], (6,8-deoxygenation of flavonoids), benzopyrans, benzofurans, (pyrrolizidine alkaloids), C10 acetylenes, etc. +; secretory canals 0[?]; (flowers bracteate); often radiate [ray florets [3 lobed], female/sterile], disc florets perfect, C shallowly lobed; anthers (free), (black), (ecalcarate), ecaudate; pollen 25.0-34.3 µm in diam., colpus ends acute, exine 2.3-4.2 µm across, with a double tectum; style hairs often rounded, only ± at style tip, stigmatic areas in two marginal bands; (achenes with phytomelan), (paleaceous); n = (4-)9-10(-19); rbcL 6bp x 4 inversion.

1135/16360: Senecio (1000), Eupatorium (1200 [s.l.] or 40 [s.s.]), Helichrysum (500-600), Artemisia (550), Mikania (430), Baccharis (400), Verbesina (300), Ageratina (290), Bidens (235), Stevia (235), Anthemis (210), Erigeron (200), Pentacalia (200), Aster (180: Flora of North America, vol. 20, 2006), Viguiera (180), Chromolaena (165), Gnaphalium (150), Solidago (150), Tanacetum (150), Olearia (130), Seriphidium (130), Ligularia (125), Achillea (115), Coreopsis (115), Anaphalis (110), Brickellia (110), Calea (110), Blumea (100), Koanophyllum (110), Euryops (100), Pectis (100), Wedelia (100), Diplostephium (90), Emilia (90), Espeletia (90: secondarily woody), Symphyotrichum (90), Felicia (85), Fleischmannia (80), Pluchea (80), Pseudognaphalium (80), Pulicaria (80), Pteronia (80), Antennaria (70-several hundred), Brachycome (70), Cremanthodium (70), Haplopappus (70), Packera (65), Perityle (65), Celmisia (60), Conyza (60), Gynoxys (60), Leontopodium (60), Metalasia (60), Monticalia (60), Parasenecio (60), Psiadia (60: polyphyletic). World-wide.

Age. Bergh and Linder (2009) suggested that diversification of Asteroideae began in the Eocene (56.6-)43.0(-29.6) m.y.a., although most estimates are somewhat younger (Funk et al. 2009c; e.g. Pelser & Watson 2009: 39-26 m.y.a.).

Synonymy: Ambrosiaceae Berchtold & J. Presl, Anthemidaceae Berchtold & J. Presl, Artemisiaceae Martynov, Athanasiaceae Martynov, Calendulaceae Berchtold & J. Presl, Coreopsidaceae Link, nom. inval., Eupatoriaceae Berchtold & J. Presl, Gnaphaliaceae Rudolphi, Grindeliaceae A. Heller, Heleniaceae Rafinesque, Helianthaceae Berchtold & J. Presl, Helichrysaceae Link, nom. inval., Inulaceae Berchtold & J. Presl, Ivaceae Rafinesque, Madiaceae A. Heller, Matricariaceae J. Voigt, Partheniaceae Link, nom. inval., Santolinaceae Martynov, Senecionaceae Berchtold & J. Presl, Tanacetaceae Vest, Tussilagaceae Berchtold & J. Presl, Xanthiaceae Vest

Evolution. Divergence & Distribution. Papers in Funk et al. (2009a) summarize biogeography, clade ages, and much more for each tribe. For fossil pollen, see Barreda et al. (2010a); depending on the identification of the grains, the first seven subfamilies in the sequence above may all have diverged by the late Eocene about 34 m.y.a.. A macrofossil, Raiguenrayun, from the Middle Eocene of Patagonia ca 47.5 m.y.a., is assignable to these clades, but not to Barnadesioideae (Barreda et al. 2010b, 2012); bird pollination was thought to be possible, yet humming birds, the iconic bird pollinators of the New World, are known only from Europe at that time (Mayr 2004). More recent age estimates have been affected by these fossils. It has been suggested that there was an (early) Oligocene radiation of the subfamilies (K.-J. Kim et al. 2005; Funk et al. 2005; Barker et al. 2008; Torices 2010). Diversification probably began in southern South America, movement fo Africa being by way of islands on what are now the Rio Grande Rise and the Walvis Ridge, indeed, it has been suggested that Asteraceae making this move may have evolved features common in island plants (Carlquist 1974) like more or less shrubby or tree-like growth forms (Katinas et al. 2013). Many clades arose in the course of a subsequent radiation from Africa (Panero & Funk 2008; Funk 2009; Funk et al. 2009c; see also Kim & Jansen 1995). Both South America and Africa are central to our understanding of the early spread and diversification of the family.

The speciose Cardueae at 2,400+ species makes up most of Carduoideae; the more basal branches are very species-poor. The tribe is now primarily Mediterranean, and Barres et al. (2013) discuss its history in some detail.

Crown Gnaphalieae (Asteroideae) can be dated to (52.3-)34.5(-20.6) m.y.a., diversification probably beginning in southern Africa, with various subsequent dispersals including one that resulted in the some 550 species of the Australasian part of the tribe (stem age [22.1-]15.6[9.1] m.y.; crown age [20.6-]14.6[-8.3] m.y. - see Bergh & Linder 2009). Within Senecio s. str. there has been intercontinental dispersal between areas with Mediterranean and desert climates (Coleman 2003), while much of the diversification in the Mediterranean-Central Asian Carduoideae-Centaureinae may be Plio-Pleistocene transition and younger (Hellwig 2004). Riggins and Siegler (2012 and references) discuss the biogeography of Artemisia, Eurasian in origin; migration here has also been extensive, while Strijk et al. (2012) look at the dispersal of polyphyletic Psiadia to Madagascar and thence to the Mascarenes.

The iconic stout-stemmed (pachycaul) giant senecios (Dendrosenecio) of the African mountains are all closely related and not immediately related to Senecio s. str. (Knox & Palmer 1995a, b; Pelser et al. 2007). Much diversification of the high-altitude species of Saussurea may have occurred in the context of the uplift of the Qinghai-Tibetan plateau within the last 14 m.y. (Y.-J. Wang et al. 2009), and there have been other radiations of Asteraceae in this area (Zhang et al. 2011 and references). Espeletia is a characteristic genus of the Andean páramo, and it, too, is often more or less pachycaul, and other Asteraceae are to be found in this habitat (Sklenár et al. 2011 and references).

For possible apomorphic characters for the family and its major clades, see e.g. Hansen (1991), Bremer (1994), Leins and Erbar (2000), Erbar and Leins (2000), Funk et al. (2009c), and Roque and Funk (2013). It is hardly surprising, given the size and ubiquity of the family, that there should be speculation about what has caused its diversification, whether the development of the capitulum itself with its high seed set, the storage of carbohydrates as unbranched-chain fructans, the diversity of secondary metabolites produced, or some other reason (see also Funk et al. 2009c). Burleigh et al. (2006) suggest that by some measures Asteraceae do show a notable shift (increase) in complexity. More attention should be paid to the significance of pollination of Asteraceae by oligolectic bees (see below). There was a palaeopolyploidy event involving most or all of the family, and again near the base of Asteroideae and within Mutisioideae. The pattern of duplicate gene retention is distinctive - structural/cell organization genes, but fewer regulatory genes were retained (Barker et al. 2008). Schranz et al. (2012) suggested that there was a lag time between the first duplication event and subsequent diversification of the family, which they thought might be causally linked.

There are perhaps parallels with Poaceae, which also have large-scale genome duplications and store carbohydrates as fructans - diversification may be best explained by focusing on particular clades in the family rather than treating the family as a unit (Schranz et al. 2012; see also, perhaps, rate shifts in S. A. Smith et al. 2011). Indeed, although Asteraceae alone contain about 8% of eudicot species, within Asteraceae, Asteroideae, the equal-youngest subfamily, include over 16,000 species, some two thirds of the family; most of the eleven clades basal to Asteroideae have relatively few to very few species (the sister clade of Asteroideae has seven species), although Cichorioideae have ca 3,600 species and Carduoideae ca 2,800 species. Net evolutionary rates within the family are highly heterogeneous (S. A. Smith et al. 2011).

Pollination Biology & Seed Dispersal.

Pollination Biology.

The capitulum can become reduced to a single flower, the single-flowered capitulae may then reaggregate into a supercapitulum, and there may occasionally be yet another round of aggregation (Claßssen-Bockhoff 1996b for details; Harris 1994 [tertiary capitulae], 1999; Leins & Gemmeke 1979; Katinas et al. 2008a). Whether a normal capitulum or some kind of supercapitulum, the whole inflorescence functions as a flower in terms of attracting pollinators, and some genes whose expression is normally restricted to individual flowers may be more widely expressed in the capitulum as a whole, as well as in vegetative shoots (Ma et al. 2008).

Pollinators of Asteraceae might seem not to be very selective, since the frequent and diverse insect visitors so obvious on a capitulum of any size trample around on top and appear to pollinate indiscriminately as they go, but this may not be quite true. Effective pollination is commonly carried out by a variety of broadly oligolectic small and often solitary bees belonging to Andrenidae (not in Australia) and Colletidae. These form complex and partly learned associations with individual species of Asteraceae; both bees and Asteraceae are common in drier areas (Linsley 1958; Moldenke 1979b; Lane 1996; Müller & Kuhlmann 2008; Kuhlmann & Eardley 2012). Moldenke (1979b) estimated that in North America about 525 bee species, well over one third of the total number of oligolectic bees, were restricted to Asteraceae. Thus within north temperate Colletes (plasterer bees) a few species specialize on Asteroideae, the other species rarely visiting them; specialization on flowers of Asteraceae has evolved three or four times there (Müller & Kuhlmann 2008). Pollination in Helianthus (sunflowers) has been particularly well studied, and several species of oligolectic bees may visit the one species of sunflower. 39 species of oligolectic bees (mostly Andrenidae and Anthophoridae) and 22 species of polylectic bes visited 21 species of Helianthus regularly for pollen, although at most few were obligately associated, but the majority worked other Asteraceae - all told, 284 species of bees visited for pollen, 128 species for nectar (Hurd et al. 1980; also Minckley et al. 1994). Similarly, Schemske (1983) noted that 11-20 species of bees, and over twice as many species of insects in general (in both cases, sometimes many more), commonly visit a single species of Asteraceae. Interestingly, pollen of Asteraceae-Asteroideae and -Cichorioideae, at least, may be unsuitable for many bees. It may lack essential amino acids, have generally lower amino acid and protein concentrations than other pollen, or contain harmful secondary metabolites (Waser et al. 1996; Müller & Kuhlmann 2008; Goulson 2010; Sedivy et al. 2011). Consequently, some bees actively avoid collecting pollen from composites, thus female bumble bees may get covered in pollen as they collect nectar, yet they do not transfer that pollen to their corbiculae (Neff & Simpson 1990; Goulson 2010), although this would not stop them being effective pollinators. In general, insect - especially bee - pollination occurs throughout the family, bird (Cronk & Ojeda 2008) and wind pollination (see below) being uncommon.

Some Asteraceae have a pump (Nüdelspritze) mechanism of secondary pollen presentation, others have a brush mechanism (see Leins & Erbar 2003b for a possibly evolutionary sequence of pollen presentation devices). Within Barnadesioideae, sister to the rest of the family, secondary pollen presentation is by simple deposition on the style/stigma (as in at least some Calyceraceae) or by an unspecialised type of brush mechanism (e.g. Erbar & Leins 2000; Leins & Erbar 2006). A number of Carduoideae, especially Centaurineae, have touch-sensitive stamens. The filaments contract when the flowers are touched by the pollinator, and the pollen is then forced out of the anther tube; this pollination mechanism appears to have arisen more than once, and is associated with short and sticky, not long and dry, stigmas and smooth, not spiny, pollen (López-Vinyallonga et al. 2009).

In wind-pollinated Asteroideae the heads have either staminate or carpellate flowers. In male heads the anthers are free and the capitulae are often pendulous, and the pollen grains have lost their spines. Since the carpellate heads may have only a single flower, the end result is a breeding system very much like that of other wind-pollinated plants like Fagales - monoecy, aggregated pollen-producing units, and female reproductive units that produce a single-seeded fruit. For the phylogeny, genome evolution, etc., of the wind-pollinated Artemisia, with its multiple invasions of the Arctic (polyploidy is apparently not involved), see Vallès and Garnatje (2005), Sanz et al. (2008) and Trach et al. (2008).

There is a great diversity of breeding systems in the family (e.g. Burtt 1961, 1977a), and the evolution of different flower types in Inuleae (Asteroideae) has been examined by Torices and Anderberg (2009). Apomixis is quite common, as in Hieracium and Taraxacum (see T. absurdum!), both in Cichorioideae, and Antennaria (Asteroideae). Dioecy has evolved from monoecy and back again in Leptinella (Cotula s.l.: Himmelreich et al. 2012).

Seed Dispersal.

Most fruits are crowned by a plumose pappus, a highly modified calyx (Yu et al. 1999: confirmation at the level of gene expression; Mukherjee & Harris 1995 and Nordenstam 2008 for variation). The hairs that make the pappus up are themselves sometimes hairy, and wind dispersal is very common. However, a number of taxa are dispersed by animals, whether by hooked fruits (Bidens), or hooks on the inflorescence (Arctium), or by myrmecochory, the fruits having some sort of elaiosome, as in Centaurea (Carduoideae) and Osteospermum (Asteroideae: Lengyel et al. 2009).

Ecology & Physiology. Growth form is notably labile in Asteraceae, and many taxa are more or less woody-herbaceous intermediates (Beaulieu et al. 2013b: character that was treated in a binary fashion, woody vs herbaceous, but c.f. e.g. Carlquist 2013); Asteraceae are common in islands, where the evolution of woodiness is common. Climbing Asteraceae are prominent in montane forests of South America (Gentry 1991).

The storage of carbohydrates as unbranched-chain fructans may contribute to the ability of Asteraceae to live in the rather dry conditions that many of them prefer (John 1996).

Flaveria (Asteroidae) has some species with C4 photosynthesis, some with C3, and some intermediate with C2 photosynthesis; details of the metabolic changes involved are quite well understood, and there have been several of these shifts (Bläsing et al. 2000; McKown & Dengler 2009; Ludwig 2011a and references, b, c; Gowik et al. 2011; Schulze et al. 2013; R. Sage et al. 2013). Christin et al. (2011b) suggest a number of dates for diversification here, and all are less than 4 m.y.a.; the repeated changes in photosynthetic mechanism may reflect an underlying "predisposition" (McKown et al. 2005), as has been suggested for the evolution of C4 photosynthesis in other groups.

Plant-Animal Interactions. The flowers of some Senecioneae and Eupatorieae are visted by male Danainae, Ithomiinae, Arctiidae and Ctenuchidae because the pyrrolizidine alkaloids they contain are used as the basis of the pheromones of these lepidoptera, or of compounds that other organisms find distasteful (see also Crotalaria and some Boraginaceae and Apocynaceae: Edgar et al. 1974; Fiske 1975; Ackery & Vane-Wright 1984; Brown 1987; Weller et al. 1999; Anke et al. 2004). Since the tribes are unrelated so there has been parallel evolution of these alkaloids within Asteroideae (e.g. Reimann et al. 2004). Pyrrolizidine alkaloids and pentacyclic triterpene saponins obtained from Asteraceae and variously modified are also found in the secretions of the defensive glands of some Chrysolina and Platyophora beetles (Chrysomelidae); both genera are very speciose (Pasteels et al. 2001; Termonia et al. 2002; Hartmann et al. 2003). Sesquiterpene lactones are also sequestered by insects (e.g. Pasteels et al. 2001). Pyrrolizidine alkaloids protect the plants that have them against some herbivores, and individual alkaloids in Senecio section Jacobaea are readily and seemingly randomly gained and lost during evolution by the switching on or off of the genes involved in their synthesis, and there is also much variation in the amount of individual alkaloids (Pelser et al. 2005).

Larvae of Nymphalidae-Melitaeini butterflies are common on Asteraceae, and also on Lamiales, from whence they probably moved less than 50 m.y.a. (Wahlberg 2001; Nylin & Wahlberg 2008; Nylin et al. 2012), a move perhaps associated with an increase in their diversification rate (Fordyce 2010). Caterpillars in a clade of Nymphalidae-Heliconiinae-Acraeini utilise primarily Andean Asteraceae, probably switching from host plants in the Passifloraceae area (Silva-Brandão et al. 2008), but in his case without a change in diversification rate (Fordyce 2010). Agromyzid dipteran leaf miners have diversified in north temperate Asteraceae; these insects prefer plants with noxious secondary metabolites (Winkler et al. 2009).

Within Carduoideae the stout root stocks and large flower heads in particular are resources for the numerous herbivorous insects that specialize on this clade. More than fifty genera of specialized thistle insects, including representatives of Zygaenidae, Tortricidae, Pterolonchidae (all Lepidoptera), Curculionidae (Coleoptera), Tephritidae (Diptera), Tingitidae (Hemiptera) and Cynipidae (Hymenoptera), are found on Carduoideae of the west Palaearctic region, although their numbers are not great considering the diversity of Carduoideae there (Zwölfer 1988; Csoka et al. 2005; Brändle et al. 2005 and literature). All these herbivores are particularly abundant in the Mediterranean region, which is perhaps where Carduoideae evolved (Zwölfer 1988). Introduced insects including a weevil and the tephritid Urophora are often very effective biological control agents of introduced Carduoideae in North America and other parts of the world (Redfern 2011). Tephritid flies are particularly noteworthy on Carduoideae, either eating fruits, exudates they induce from the plant, or forming galls in the stem or inflorescence (Korneyev et al. 2005, esp. Urophora; Redfern 2011). They are also common on other species of the family pretty much world-wide (e.g. Prado & Lewinsohn 2004; Norrbom et al. 2010), and tephritid-induced ball galls on the stems of Solidago growing in the prairies of North America are conspicuous in the late summer (Abrahamson & Weis 1997). Interestingly, Prado and Lewinsohn (2004) found that related species of Asteraceae in the Espinhaço mountains or Minais Gerais, Brazil, tended to support a similar tephritid fauna which, however, might not be made up of immediately-related taxa.

Bacterial/Fungal Associations. Ectomycorrhizae have been reported from a number of Australian Gnaphalieae (Warcup 1990), but this work has apparently not been extended. The oomycete Pustula, a white blister rust, is found quite widely on Asteraceae, with a few occurrences on Goodeniaceae, Araliaceae (Trachymene) and Gentianaceae (Ploch et al. 2010b).

Genes & Genomes. For genome duplications, see Barker et al. (2008) and Schranz et al. (2012). A large inversion in the chloroplast genome occurs in most of the family, but not Barnadesioideae and other Asterales, and its discovery in the early days of molecular systematics was very exciting, in part because it was consistent with a morphological phylogeny that came out at about the same time (c.f. Jansen & Palmer 1987; Bremer 1987; see also Y.-D. Kim & Jansen 1995; K.-J. Kim et al. 2005; Timme et al. 2005). Much, but not all, of the uncertainty in relationships around the old Mutisioideae seems to have been resolved, with distinctive gene deletions and insertions characterising a number of the clades (Panero & Funk 2008).

Relatively common and wide (with respect to both taxonomy and current geography) hybridisation in Asteroideae in particular is shown by incongruence between topologies based on different genomes, and this makes life for those involved in phylogeny reconstruction rather interesting (e.g. Fehrer et al. 2007; Pelser et al. 2008, 2010, 2012; Soejima et al. 2008; Morgan et al. 2009; Montes-Moreno et al. 2010; Schilling 2011; Smissen et al. 2011; Calvo et al. 2013). Thus there is significant incongruence between relationships suggested by plastid and nuclear sequences in Senecioneae, probably due to ancient hybridisation rather than incomplete lineage sorting (Pelser et al. 2010). Smissen et al. (2011) suggest that complex allopolyploidy may have been involved in the origin of at least four clades in Gnaphalieae, one of which is now globally distributed and that together encompass more than half the ca. species of the tribe. For some wide hybridization - between members of different subtribes - in Cichorioideae, see Y. Liu et al. (2013). Vallès et al (2012) discuss polyploidy and its connection with genome size, etc., while Vallès et al. (2013) summarize genome size variation in the family, although unfortumnately little is known about the basal pectinations.

Economic Importance. Timme et al. (2007) provide a phylogeny of the important genus Helianthus; Simpson (2009) summarised what is known of the otherwise rather slight economic importance of the family.

Chemistry, Morphology, etc. For a general entry into the literature of Asteraceae, see papers in Funk et al. (2009a) - there is a helpful glossary; Anderberg et al. (2006) also summarize the variation in the family.

There are tens of thousands of secondary metabolites produced by the family (Calabria et al. 2009 for a convenient summary and entry into the literature), although nothing seems to be known about the secondary chemistry of Hecastocleioideae and Gymnarrhenoideae. See Seaman (1982) for sesquiterpene lactones, Zidara (2008) for those of Cichorieae, Seaman et al. (1990) for diterpenes, Aniszewski (2007) for alkaloids, and Bohm and Stuessy (2001: family) and Sareedenchai and Zidorn (2010: Cichorieae) for flavonoid chemistry; Calabria et al. (2007) produced a phytochemical phylogeny at the tribal level. Sesquiterpene lactones give the bitter taste of many Asteraceae, e.g. Cnicus benedictus.

The distinctive capitulate inflorescence of Asteraceae lacks a terminal flower and is basically racemose, unlike in its immediate relatives (Pozner et al. 2012). In Gorteria the outermost (ray) flowers develop both centrifugally and more slowly than the acropetally-developing more central (disc) flowers (Philipson 1953, Harris 1995 and references; Leins & Erbar 2003b; Thomas et al. 2009), and there are several cases where the peripheral flowers develop more or less centrifugally (literature summarized by Pozner et al. 2012). Interestingly, those Calyceraceae which have an inflorescence most similar to that of Asteraceae, and those Asteraceae with some centrifugal development of flowers that can perhaps be linked with the cymose part inflorescences common in the outgroups to Asteraceae, are both derived within their respective families (c.f. Pozner et al. 2012). There are floral bracts in some Asteroideae-Heliantheae (the tribe includes taxa that were in Eupatorieae), but they seem to have been reacquired more than once and are certainly not plesiomorphic in the family as was once thought (see e.g. Harris 1995 for literature). The involucral bracts in Asteroideae-Senecioneae are uniseriate.

The pappus (modified calyx) is often not the first part of the flower to be initiated, and it may start to develop well after the corolla (see Mukherjee & Harris 1995, Nordenstam 2008), although otherwise the sequence of initiation of flower parts is as might be expected. In general, the very different adult floral morphologies are quite similar early in development (Harris 1995). A corolla ring primordium may initate first, or petals may be initiated separately, i.e., there is variation between early and late corolla tube development, the former perhaps being derived (Harris 1995: Leins & Erbar 2000; Erbar & Leins 2000 for floral development). CYC-like genes appear to be expressed in the abaxial petals here, rather than in the adaxial petals, as in other core eudicots (Citerne et al. 2010).

Although floret morphology varies extensively in Asteraceae, this needs to be put in the context of a tree. Koch (1930 and references) and Manilal (1971) discussed corolla venation; the corolla of the ray flowers of some Asteroideae may even be unvascularized. Many Asteroideae have three-toothed ray florets that give the appearance of being slit-monosymmetric, but they may be a modified 2:3 bilabiate corolla in which the adaxial lobes have been suppressed (Weberling 1989; Gillies et al. 2002); slit-monosymmetric flowers are occasionally found in the family. Some taxa, including Barnadesioideae, have a midvein in the petal (see also Carlquist 1976; Gustafsson 1995). The corolla hairs of Barnadesioideae are distinctive: The epidermal cell is undistinguished, the basal cell is short and thick-walled, and the other cell is longer and has thin walls. There is variation in the orientation of the gynoecium and style branches: carpels superposed, style branches arranged radially to the head surface; carpels collateral, style branches tangential to head surface: see Robinson 1984); details of the distribution of this feature are unknown. Buphthalmum has a hollow style (Leins 2000); I do not know how widespread such styles are in Asteraceae.

There is much variation in pollen morphology in the family, and this has often been described in terms of pollen "types". However, Blackmore et al. (2009) decompose these types into a number of individually-varying characters, and then discuss the distribution of some of these characters across the Asteraceae tree. Caveate pollen is found in Arctoteae and some Lactuceae, and may be more basal on the tree than it is placed here (as a synapomorphy for [Corymboideae + Asteroideae]). Indeed, Blackmore et al. (1984) noted that it is evident early in development in Gerbera (Mutisieae), but not later, and suggested that pollen grains of Asteraceae might all be basically caveate - however, the very definition of caveate is unclear (Blackmore et al. 2009). Wortley et al. (2007b) used distinctive pollen characters to help place some genera whose relationships had previously been unclear. See also Skvarla et al. (1977: pollen terminology in Asteraceae), Roque and Silvetstre-Capelato (2001: pollen of Gochnatioideae), Wortley et al. (2008: Arctotidae-Cichoridoideae), Wortley et al. (2009: comprehensive bibliography of palynological work in the whole family), Tellería and Katinas (2009: Mutisia), Osman (2009: Cichorioideae-Cardueae), Hong Wang et al. (2009b and references: Cichorioideae-Cichorieae).

The seed coat is poorly developed, as might be expected; there may be calcium oxalate crystals in the inner layer (Guignard 1893). Guignard (1893) also suggested a), that the ovules may be vascularized, and b), that there is sometimes an antiraphe, as in Centaurea. Asteroideae-Heliantheae have distinctive black fruits that are covered by phytomelan (see Graven et al. 1998 for what is known about this compound); they are also described as being carbonized. Nuclear endosperm is sometimes mentioned as being the only endosperm condition found in the family or as a synapomorphy for it (e.g. Tobe & Morin 1996; Inoue & Tobe 1999), but there is in fact considerable variation in endosperm development (Dahlgren 1920; Johri et al. 1992 for references). The embryo of Syneilesis may lack cotyledons entirely (Teppner 2001). For fatty acids in the seeds, see Bamai and Patil (1981). For embryo sac development, which I have not thought about, see e.g. Fagerlind (1939c): there are embryo sacs other than the common monosporic 8-nucleate type. For chromosome reduction in Gnaphalieae, e.g. from n = 12 to n = 3 in Podolepis, see (Smissen et al. 2011 and references).

For general information on Asteraceae, see e.g. Carlquist (1976: variation in the context of a tribal classification), K. Bremer (1987, esp. 1994: the classification rather different from that above, 1996: subfamilies), Hind et al. (1996), and Jansen et al. (1991: variation in the context of phylogeny). See also Goldflus (1898-9: antipodal cells), Harris (1995: inflorescence and flower development), Watanabe et al. (2007) and Semple and Watanabe (2009), chromosome numbers, Katinas et al. (2008b: Mutisioideae in the old broad sense - general morphology), Thomas et al. (2009: development of Gorteria flowers), and Wist and Davis (2006: nectaries and nectar secretion).

Phylogeny. There has been much phylogenetic work on Asteraceae, and only a few references are included. Panero and Funk (2002, especially 2008; see also Funk et al. 2005, a supertree, 2009c, a metatree) present the phylogeny reflected in the classification above. Gymnarrhena was excluded from Asteroideae by Anderberg et al. (2005). For resolution of much of the uncertainty in relationships around the old Mutisioideae, see Panero and Funk (2008); morphological data suggested to Roque and Funk (2013: character states tricky) that Wunderlichioideae and Stifftioideae might form a clade.

For phylogenetic relationships within Barnadesioideae, see Urtubey and Stuessy (2001) and in particular Gustaffson et al. (2001), Gruenstaeudl et al. (2009) and Funk and Roque (2011); the position of Schlechtendalia is uncertain. For corolla morphology in this subfamily, see Stuessy and Urtubey (2006).

For a phylogeny of Carduoideae-Cardueae, see Garcia-Jacas et al. (2002), Susanna et al. (2006) and Park and Potter (2013). Carduinae are paraphyletic, but for a phylogeny of the monophyletic Centaureinae, see Garcia-Jacas et al. (2001) and Hellwig (2004). For relationships in Echinops, see Garnatje et al. (2005: sectional classification) and Sánchez-Jimenéz et al. (2010), and for those within Cousinia (biphyletic) and relatives, see López-Vinyallonga et al. (2009).

Within Cichorioideae, Warionia may be sister to all other Cichorieae (Kilian et al. 2009); although no flavonoids have been reported from them, they are diverse in the rest of the tribe (Sareendenchai & Zidorn 2010 - see Zidorn 2008 for sesquiterpene lactones there). Subtribes are monophyletic, although Faberia seems to be a hybrid between a member of Crepidinae and Lactucinae (it looks more like the latter), but relationships between them are only partly resolved (Y. Liu et al. 2013). In Sonchinae, Sonchus is para/polyphyletic (Kim et al. 2007), with woody, island-dwelling forms being independently derived within the clade. The classic studies by Babcock (e.g. 1947) on Crepis that assumed that evolution - in this case of the karyotype in particular - was unidirectional need comprehensive re-evaluation (Enke & Gemeinholzer 2008). Species limits around here are difficult because of apomixis; see Gottschlich (2009) for the complexities of variation in Hieracium in a smallish area of Italy. For a phylogeny of Tragopogon and its relatives, see Mavrodiev et al. (2005), and of the African Gorteriinae, see Funk and Chan (2008). For a phylogeny of Vernonia (Vernonieae), a genus whose circumscription is problematic - either it is huge, or quite small - see Keeley et al. (2007), and for that of the largely Peruvian Liabeae, sister to Vernonieae, see Funk et al. (2012).

Within Asteroideae, North American Astereae are monophyletic and largely herbaceous (Noyes & Rieseberg 1999), however, Aster is extensively para/polyphyletic, and its limits are now restricted (e.g. Li et al. 2012); for Machaerantherinae, see Morgan et al. (2009). For the Hinterhubera group, see Karaman-Castro and Urbatsch (2009: groupings geographic); Olearia is likely to be polyphyletic (Cross et al. 2002). Strijk et al. (2012) find that Psiadia (and Conyza) are also polyphyletic. For the phylogeny of the helenioid Heliantheae, see Baldwin et al. (2002), Morphological relationships in Inuleae and Plucheeae are discussed by Anderberg (1991b, c); for the phylogeny of Inuleae (inc. Plucheeae), see Anderberg et al. (2005) and Englund et al. (2009). For a phylogeny of Anthemidae in the southern hemisphere, see Himmelreich et al. (2008 and references), Cotula is not monophyletic (Himmelreich et al. 2012) and will probably need to be expanded, and for a delimitation of Anthemis itself, see Lo Presti et al. (2010); for circum-Mediterranean Anthemidae, also their biogeography, see Oberprieler (2005), for Chrysanthemum and other Anthemidae, see Zhao et al. (2010), and for Tanacetum, see Sonboli et al. (2012: little resolution). For relationships within and the evolution of Artemisia, see Vallès et al. (2003) Vallès and Garnatje (2005), Sanz et al. (2008), Pellicer et al. (2010b: genome size, etc., 2011), Garcia et al. (2011: North American taxa) and Riggins and Siegler (2012: paraphyly, etc.). For the phylogeny of the helenioid Heliantheae, see Baldwin et al. (2002), and for that of the iconic Hawaiian silverswords and their immediate relatives, and their relatives in turn - west North America tarweeds (Helenieae-Madiinae) - see Baldwin and Wessa (2000) and Carlquist et al. (2004, also Madiinae Showcase). Bidens on Hawaii also shows much variability in growth form, etc., but there is little molecular variation or genetic barriers between the species (Ganders et al. 2000). Within Gnaphalieae, morphological variation is analyzed by Anderberg (1991a), and phylogenetic relationships there have begun to be disentangled by Bayer et al. (2000). Helichrysum is polyphyletic (Galbany-Casals et al. 2004, 2009; Bergh & Linder 2009); Ward et al. (2009), Galbany-Casals et al. (2010), Montes-Moreno et al. (2010), Nie et al. (2013: Anapahalis embedded in Helichrysum) and Bengtson et al. (2014: the South African Metalasia) further clarify relationships in this tribe. Relationships within Senecioneae, particularly the huge genus Senecio, are beginning to be disentangled (Pelser et al. 2006, esp. 2007, see also Pelser et al. 2010; Calvo et al. 2013); for relationships within Euryops, see Devos et al. (2010). For Symphyotrichum and relatives, see Vaezi and Brouillet (2009). Within Inuleae, the sections of Blumea need overhaul, see Pornpongrungrueng et al. (2009).

Classification. See Panero and Funk (2008) for the subfamilial classification above (there are, of course, alternative classifications - e.g. Jeffrey 2004); it is similar in basic structure to that in Funk et al. (2009b: as 43 tribes, tribal, etc. classifications, see the accounts there). Anderberg et al. (2006) have recently enumerated the genera in the family. However, generic limits in many places are in a state of flux. Vernonia is a classic case of uncertainty - should it include 800-1000 species, or should these species be placed in 20 subtribes, of which two thirds of the genera are mono- or ditypic? (Keeley et al. 2007 for a phylogeny; Robinson 2006 and references for genera). Should there be lumping or splitting in the even larger genus Senecio (see Pelser et al. 2006, esp. 2007)? In the latter case, Senecio species are found in over eight clades, but even so Senecio s. str., at ca 1,000 species, is paraphyletic (Pelser et al. 2007). Substantial adjustments to generic limits will also be needed in Asteroideae-Inuleae-Inulinae (Englund et al. 2009) and in Astereae (e.g. Li et al. 2012). Finally, hybridisation (see above) makes some genera and even subtribes non-monophyletic.

Botanical Trivia. Arctium lappa (burdock) infructescences became attached to the dog of a Swiss engineer, George de Mestral, in 1945, and the result was the development of velcro (Wikipedia 2009).

Thanks. I am grateful to Jose L. Panero for comments.