EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; nuclear genome size [1C] <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA gene moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; pro- and metaphase spindles acentric; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [only neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; 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 +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= 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, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, 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], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; 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, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen 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, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [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, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome size [1C] <1.4 pg [mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; 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, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[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]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; 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 [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; 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.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, 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]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ 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, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).
[BERBERIDOPSIDALES [SANTALALES [CARYOPHYLLALES + ASTERIDS]]] / ASTERIDS ET AL. / SUPERASTERIDS : ?
[SANTALALES [CARYOPHYLLALES + ASTERIDS]]: ?
[CARYOPHYLLALES + ASTERIDS]: seed exotestal; embryo long.
ASTERIDS / ASTERIDAE / ASTERANAE Takhtajan: nicotinic acid metabolised to its arabinosides; (iridoids +); tension wood decidedly uncommon; C enclosing A and G in bud, (connate [sometimes evident only early in development, petals then appearing to be free]); anthers dorsifixed?; if nectary +, gynoecial; G , style single, long; ovules unitegmic, integument thick, endothelium +, nucellar epidermis does not persist; exotestal [!: even when a single integument] 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 / EUASTERIDS: plants woody, evergreen; ellagic acid 0, non-hydrolysable tannins not common; vessel elements long, with scalariform perforation plates; nodes 3:3; sugar transport in phloem active; inflorescence usu. basically cymose; flowers rather small [<8 mm across]; C free or basally connate, valvate, petals often with median adaxial ridge and inflexed apex; A = and opposite sepals or P, (numerous [usu. associated with increased numbers of C or G]), free to basally adnate to C; G #?; ovules 2/carpel, apical, pendulous; fruit a drupe, drupe ± flattened, surface ornamented; seed single; duplication of the PI gene.
ASTERID II / CAMPANULIDAE:myricetin 0; style shorter than the ovary; 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 and Magallón et al. (2015: note topology) an age of around 93.7 m.y., Bremer et al. (2004: note topology) an age of ca 114 m.y. and Wikström et al. (2015: note topology) an age of (110-)101(-90) m.y., Foster et al. (2016a: q.v. for details) an age of around 98 m.y., Bell et al. (2010: note topology) ages of (94-)84, 77(-69) m.y., Nylinder et al. (2012: suppl.) an age of ca 68.8 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.; the age of this node is around 111 m.y. in Z. Wu et al. (2014: note topology).
Divergence & Distribution. Divergence at this node probably occurred in plants growing in the southern hemisphere (Beaulieu et al. 2013a).
Taxa with relatively small flowers that are aggregated into conspicuous flower-like inflorescences (but c.f. Campanulaceae, etc.; see Leins & Erbar 2010: fig 157) are common in all three large orders in this clade, the apices of the petals tend to be pointed (not in Aquifoliaceae), and valvate corollas are common. The feature "small flowers" itself may be assignable to the euasterid node, since the first nodes of both the lamiid and campanulid clades may have this feature.
Changes in seed size may be pegged to this node. Seeds of this clade are generally rather small, perhaps connected with the herbaceous-shrubby habit so common here, and contrast with the larger seeds of most Aquifoliales, Icacinales, etc. (see also Moles et al. 2005a). Endress (2011a) suggested that an inferior ovary might be a key innovation here (but see below).
The position of early initiation of the corolla tube on the tree is uncertain. Although a number of families show this kind of initiation, not only is sampling within the larger orders poor and within the smaller orders largely non-existent, in the lamiids both Oleaceae and Rubiaceae, basal or almost so in their orders (Lamiales and Gentianales respectively), may have early initiation, and corolla initiation in Aquifoliales and basal clades in the lamiids is largely unknown (Leins & Erbar 2003b for a summary). Furthermore, there may be a developmental connection between early corolla tube formation and the way inferior ovaries in the campanulids develop (Ronse Decraene & Smets 2000). Taxa with more or less superior ovaries are scattered throughout the campanulids, e.g. Sphenostemon (Paracryphiales-Paracryphiaceae), Pittosporaceae (Apiales), Rousseaceae-Carpodetoideae and Phellinaceae (Asterales), within Bruniales, etc., while in Adoxaceae, sister to other Dipsacales, the ovary is semi-inferior, Ying et al. (1993) even describing the ovary of Tetradoxa as being superior, so it will be interesting to see if corolla development changes accordingly.
Chemistry, Morphology, etc. Acetylenic fatty acids/polyacetylenes are sporadic in this clade (e.g. Erbar & Leins 2004; Leins & Erbar 2004b), occurring in Asterales, Dipsacales and Apiales, but always in much embedded clades. These similarities are probably parallelisms. Although iridoids and polyacetylenes usually do not co-occur, the two may be found together, as in Torricellia angulata (Pan et al. 2006; Liang et al. 2009).
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.
ASTERALES Link Main Tree.
(Route I secoiridoids +, (fructan sugars accumulated as isokestose oligosaccharides [inulins]), starch generally 0; apotracheal parenchyma 0; leaves spiral; flower size?; C valvate, petal apiculi inflexed; A (basifixed), free from C; pollen grains often tricellular; orbicules 0; nectary +; style long; ovules many/carpel, integument <7 cells thick, endothelium +, hypostase 0; antipodal cells ephemeral; embryo suspensor filamentous, micropylar and chalazal endosperm haustoria +; x = 9; 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, not too different from the (94-)82(-71) m.y. that Wikström et al. (2015), the (98.2-)84.5(-71.4) m.y. that Tank and Olmstead (2017) and the ca 83.7 m.y. that Tank et al. (2015: Table S1) were to suggest considerably later, Bremer et al. (2004) suggested around 93 m.y., while estimates in Janssens et al. (2009) are 94±11.2 m.y. old. Magallón and Castillo (2009) estimate an age of (84.7-)84.5, 84.3(-84.1) m.y., Magallón et al. (2015: note topology) an age of ca 83.2 m.y., and Beaulieu et al. (2013a: 95% HPD) thought that the crown clade was (101-)89(-79) m.y. old. At (113.6-)106.6, 93.2(-87.9) m.y., ages in Barreda et al. (2015: table S2) tend to be a little older, although one at (83.2-)81.1(-78.9) m.y. was something of an outlier.
Note: Boldface denotes possible apomorphies, (....) denotes a feature common in the clade, exact status uncertain, [....] includes explanatory material. Note that the particular node to which many characters, particularly the more cryptic ones, should be assigned is unclear. This is partly because homoplasy is very common, in addition, basic information for all too many characters 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 are the not-so-trivial issues of how character states are delimited and ancestral states are reconstructed (see above).
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 relationships within Campanulaceae are 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), and the like, 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); this work needs to be extended. Monosymmetry is often associated with a slit the length of the corolla, i.e. is the 0:5 type. 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 and development, see Philipson (1953) and Harris (1999), for fructans/inulins, see e.g. Pollard and Amuti (1981) and Meier and Reid (1982), for integument thickness, see Inoue and Tobe (1999), and for pollen, see Polevova (2006). For general discussions of variation in the order, see J. Kadereit (2006) and Lundberg (2009).
Phylogeny. For the relationships of Asterales, see the asterid IIclade. Extensive phylogenetic structure in Asterales, although often with rather weak support, was early apparent (Gustaffson & Bremer 1997; 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 were also associated. Donatia itself is there very weakly linked with Alseuosmiaceae et al., and in some studies it is sister to Abrophyllum (Carpodetaceae: Gustafsson et al. 1997), not to Stylidiaceae. Stylidiaceae and Donatiaceae are weakly (D. Soltis et al. 2000) or quite strongly (Kårehed et al. 2000; Lundberg 2001; Tank & Donoghue 2010) supported as sister taxa.
There were suggestions that Rousseaceae, Pentaphragmataceae and Campanulaceae were 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. 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.
Relationships between Asteraceae and its immediate relatives also vary somewhat according to the gene studied (A.P.G. 2003 for references). Menyanthaceae did not link with the other three families in the four-gene study of Albach et al. (2001b). Leins and Erbar (2003b) thought that Goodeniaceae were 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, while Soltis et al. (2007a) found the relationships [[Calyceraceae + Goodeniaceae] Asteraceae]. 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 [Phellinaceae [Alseuosmiaceae + Argophyllaceae]] clade.
Previous Relationships. The Asterales here are basically Takhtajan's (1997) Asteridae, but with the addition of sundry Hydrangeales. Cronquist (1981) also placed many families here in Asterales in the orders placed towards the end of his Asteridae, although some families were also in his 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]: inflorescence terminal; A free.
Age. Wikström et al. (2001) suggested an age of (86-)81, 76(-71) m.y. for this node, Tank et al. (2015: Table S1, S2) ages of about 76.2 to 81.4 m.y., Magallón et al. (2015) an age of around 76 m.y. and Crowl et al. (2016) (86-)76(-67) m.y., about the same. J. Lundberg (in Hansen & Müller 2009) estimated an age of anywhere from 100 to 20 m. years.
ROUSSEACEAE Candolle Back to Asterales
Young stem with separate vascular bundles; lamina margins gland-toothed; anthers basifixed, ?extrorse; G , opposite petals; integument 5-8 cells across.
4[list]/13 - two subfamilies below. Mauritius, scattered from New Guinea to New Zealand.
1. Rousseoideae Horaninow
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, large [2< cm long], (4-merous); K valvate, C connate; anthers 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; exotesta thick-walled, other cells crushed; micropylar haustorium +, embryo medium-long; n = ?
1/1: Roussea simplex. Mauritius (map above: green). [Photo - Flower © D. Lorence]
2. Carpodetoideae J. Lundberg
Trees; chemistry?; vessel elements with scalariform perforation plates; nodes 1:1, 3:3; petiole bundles arcuate or annular plus accessories; stomata anomocytic; hairs unicellular, thick-walled, strongly curved, warty; inflorescence paniculate; flowers small [<8 mm across/long], 4-6-merous; C free; A free or adnate to base of C, (dorsifixed - Cuttsia); (pollen in tetrads - Carpodetus); G [(3-6)], (± inferior - Carpodetus), style medium (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 small; n = 14, 15.
3/12. New Zealand, E. Australia, Halamahera to Vanuatu (map from Pillon et al. 2014; Australia's Virtual Herbarium xii.2014: above, red). [Photo - Inflorescence.]
Synonymy: Abrophyllaceae Nakai, Carpodetaceae Fenzl
Evolution: Divergence & Distribution. Mauritius is only some 8 m.y.o. - what was the history of Roussea over the preceding ca 70 m.y. (Lundberg 2001a)?
Pollination Biology. Roussea is pollinated by the gecko Phelsuma. The pollen is embedded in a slimy substance and sticks to the gecko, which may also disperse its seeds, which are embedded in pulp (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.
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).
For further details of vegetative anatomy of Carpodetoideae, see Gornall et al. (1998: as Escalloniaceae) and Carlquist (2012c), indumentum, see Al-Shammary and Gornall (1994), floral morphology, see Tobe and Raven (1999), and seed anatomy, see Takhtajan (2000). For anatomy of Roussea, see Watari (1939), Ramamonjiarisoa (1980) and Gornall et al. (1998: as Escalloniaceae). For some general information, see Gustaffson and Bremer (1997) and Koontz et al. (2006: Roussea).
Phylogeny. [Carpodetus [Cuttsia + Abrophyllum]] is the strongly supported set of relationships within Carpodetoideae (Gustaffson & Bremer 1997; Lundberg 2001a; Pillon et al. 2014).
Classification. Species limits in Carpodetus need attention.
Previous Relationships. Rousseaceae were previously of uncertain position. Takhtajan (1997) placed Roussea (as Rousseaceae) in Rosidae-Celastranae-Brexiales, and Carpodetoideae have often been associated with Saxifragaceae s.l., i.e. the woody Saxifragaceae, thus Takhtajan's Carpodetaceae were members of his heterogeneous Hydrangeales (see also summary in Lundberg 2001a). No members of the family were 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; fructan sugars accumulated as isokestose oligosaccharides [inulins], 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 racemose; flowers large, (3-)5(-10)-merous, monosymmetric; resupinate [median sepal abaxial], C with early tube formation, connate; flowers protandrous, anther dehiscence in bud, connivent, introrse, at least initially close to stigma, [secondary pollen presentation]; pollen (bicellular), prolate, endexine throughout, not lamellate; G , sub/inferior, (placentation parietal), placentae intrusive, bilobed, style elongating after anthesis, with hairs at tip, stigma lobed; integument ca 6 cells across; fruit a capsule, K persistent; seeds many, small [usu. <200 µg]; exotesta cells lignified, polygonal or elongated, (endotestal cells, esp. inner walls, thickened); endosperm (starchy), copious; x = 9; expansion of chloroplast inverted repeat into small single copy region, 5bp ndhF deletion, rpl23 duplication/transposition, chloroplast infA and accD genes 0 [but see Haberle et al. 2008a], biparental plastid transmission [?levels], mitochondrial coxII.i3 intron 0.
84[list]/2,380. World-wide - five subfamilies below.
Age. Bell et al. (2010) estimated a crown group age of (67-)56, 53(-41) m.y. for the family, Wikström et al. (2001) suggested an age of (62-)59, 46(-43) m.y., Knox (2014) an age of around 60 m.y., while (72-)64(-56) m.y. is the estimate in Crowl et al. (2016).
[Cyphioideae + Campanuloideae]: style ?hollow, hairs with bulbous bases; fruit a septicidal capsule.
1. Cyphioideae Schönland
Perennial herbs (twining vines), shrubs, with tuberous roots; (flowers single); C ± monosymmetric, 3:2, early sympetaly; filaments largely free or connate, (anthers slightly coherent); pollen psilate; G semi-inferior, style bends away from median K, no elongation after A dehiscence, pollen deposited in pollen box, base of box stigmatic head, stylar canal +[?], fluid-filled cavity at end of style with a lateral (terminal) pore; ?embryology; capsule septi- and loculicidal [valves bifid]; (seeds winged); n = 9.
1/65. Especially South Africa, also east Africa (map: from Thulin 1978).
Age. (33-)14(-22) m.y. is the estimate for the age of crown-group Cyphioideae in Crowl et al. (2016).
Synonymy: Cyphiaceae A. de Candolle
2. Campanuloideae Burnett
Perennials (annuals), roots often thick; polyacetylenes + [14-C aliphatic tetrahydropyran derivatives - ?elsewhere], caffeic acid, p-coumaric acid +, latex rich in polysterols; (vessel elements with scalariform perforation plates); palisade mesophyll with arm cells; inflorescence often ± cymose/determinate; flowers polysymmetric; median K adaxial; stamens sprawling at bottom of corolla tube after anthers have dehisced, persistent bases conceal nectar; pollen spheroid to oblate-spheroid, verrucate or with spicules; G [(2-)3(4-10)], (superior-)inferior, opposite sepals (C), or median member adaxial, long-hairy, especially in the upper half or so, hairs retractile [presenting pollen before retraction], 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.
50/1,050. More or less world-wide, especially Old World, few in the Antipodes and South America (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), (56-)43, 41(-28) m.y. (Bell et al. 2010), and around 60 m.y. (Knox 2014: Monopsis sister to rest); other ages are (41-)37.4-23.5(-3.2) m.y.a. (Roquet et al. 2009) and some 26.3-15.8 m.y.a. (Wikström et al. 2001), or rather later, ca 50.55 m.y.a. (Crowl et al. 2014: Platycodon sister to the rest) and (61-)53(-46) m.y.a. (Crowl et al. 2016). An age for stem Campanuloideae is ca 41 m.y.a. (Wikström et al. 2001: sister to what?).
2A. Cyanantheae Meisner
Leaves often opposite; (A 3); pollen colpate/colporate; G , opposite ?; (fruit a berry); n = 7-9 (17).
10/60: Codonopsis (23), Cyananthus (23). Old World: Central Asia to West Malesia, few in Canaries and N. Africa, often (sub)tropical, not Europe or northern Asia.
Synonymy: Cyananthaceae J. Agardh
[Wahlenbergieae + Campanuleae]: pollen porate, (flattened-triangular); epicotyl and hypocotyl usually not elongated.
2B. Wahlenbergieae Endlicher
(Leaves opposite); n = 7-9, 17.
?: Wahlenbergia (260). Especially Africa and Australia.
2C. Campanuleae Dumortier
Fruit dehiscing laterally by pores or slits [caused by activity of axicorn on drying], (indehiscent); n = 6-11, 13, 15, 17.
?: Campanula (420), Adenophora (65). Especially N. temperate Old World, very few in the Antilles.
Synonymy: Jasionaceae Dumortier
[Lobelioideae [Cyphocarpoideae + Nemacladoideae]]: ?
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 [so median C abaxial], (not); C (3:2), 2:3, 0:5 [split-monosymmetric], (spurred - Heterotoma), (fenestrate); (A 3 + 2 staminodes), filaments connate at least apically, anthers connate; pollen reticulate-striate; style elongating, with brush hairs, pollen in pollen box [pump mechanism: Nüdelspritze], stigma wet; synergids hooked, (antipodal cells barely persistent); fruit dehiscing laterally, (capsule loculicidal), (circumscissile), (fruit fleshy); n = (6-)7(-13).
29[notional]/1,200: 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 - e.g. (59.6-)54.9(-50.9) m.y. (penalized likelihood) versus (88.2-)72.7(-52.2) m.y. (BEAST: see Antonelli 2009); another estimate is (65-)57(-49) m.y. (Crowl et al. 2016).
Synonymy: Dortmannaceae Ruprecht, Lobeliaceae Jussieu, nom. cons.
[Cyphocarpoideae + Nemacladoideae]: fibrillar protein intranuclear inclusions; n = 9.
4. Cyphocarpoideae Gustafsson
Annual to perennial herbs; leaf margins deeply lobed, spiny; ?inflorescence; C induplicate-valvate, 1:4, adaxial petal cucullate, with apical appendage; A epipetalous, not connate, but flowers poorly known; ovary notably elongated; ?embryology; fruit dehiscing laterally, ?loc.
5. Nemacladoideae M. H. G. Gustafsson
Tiny annuals (one sp. perennial); flowers small [<5 mm across]; C 3:2; A (adnate to C), fimbriate/digitate to entire ?nectaries at outside bases of adaxial filaments, filaments free basally or not, at least connate apically, (2 with adaxial appendage), anthers (spreading); pollen (6-colpate), spheroid to oblate-spheroid, verrucate or with spicules; large "glands" at base of style; G also , half inferior to superior, style hairs retractile [?], style bending towards or away from median K; ?embryology; (fruit circumscissile - N. californicus).
1-2/25: Nemacladus (24). S.W. U. S. A., esp. California, Mexico (map: from Wimmer 1968).
Age. A suggested age for crown-group Nemacladoideae is (59-)44(-27) m.y. (Crowl et al. 2016).
Synonymy: Nemacladaceae Nuttall
Synonymy: Cyphocarpaceae Reveal & Hoogland
Evolution: Divergence & Distribution. Knox et al. (2006, no Nemacladoideae 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, indeed, the whole family is likely to have spread from from Africa following the K/P extinction events, land bridges and island hopping rather than continental drift being the likely means of dispersal (Crowl et al. 2016). For ages of various clades within Campanulaceae, see Roquet et al. (2009); ages for deeper nodes in different analyses varied considerably. Crowl et al. (2014) give dates for branching points within Campanuloideae, but note details of the topology there.
The biogeographic history of Campanuloideae 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. Nearctic Campanuloideae got there from the Palaearctic (c.f. Lobelioideae: Crowl et al. 2016). There are several remarkable disjunctions, 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 other species of the genus sampled.
Lobelioideae moved to the Neotropics from Africa several times, with some nine subsequent dispersals to the Nearctic and five in the reverse direction (Crowl et al. 2016). 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; Crowl et al. 2016); Fetene et al. (1998) discuss the physiology of these plants in the context of living in the afro-alpine environment, and suggest that the advantage of the caulescent habit is that the plants - at least, the growing part - inhabit a more favourable microclimate with less extreme temperatures. 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 study. Moreover, giant lobelias in Bhutan and Hawaii represent independent acquisitions of the habit, and the former, L. nubigena, is the only known member of a clade (15-)13.8(-12.6) m.y.o., rather older than the ages of the other giant lobelias which tend to be younger than the habitats in which they live (L.-Y. Chen et al. 2016). Tetraploid chromosome numbers predominate in woody Lobelioideae in general (Lammers 1993; Crowl et al. 2016). 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; see also L.-Y. Chen et al. 2016).
Well over half the diversity in Lobelioideae is represented by two radiations that have occurred within the last 15 m.y. or so. There has been extensive diversification in the Siphocampylus-Burmeistera-Centropogon-Lysipomia clade in South America, particularly along the Andes; the Chilean Lobelia section Tupa is sister to the whole group, Lysipomia includes ca 40 rosulate species with small to minute (ca 3 mm across, the size of the whole plant of L. mitsyae) and sometimes almost polysymmetric flowers growing in the páramo, while the Siphocampylus-Burmeistera-Centropogon clade, the centropogonids, includes around 550 species (West & Ayers 2006; Sklenár et al. 2011; see also Knox et al. 2008; Antonelli 2008; Lagomarsino et al. 2014). Diversification of the whole clade began 18-15 m.y.a. along with the elevation of the Andes, and the 550+ centropogonids are the result of a radiation that began 12 m.y.a., peaking ca 5 m.y.a. (Pennington et al. 2010; Lagomarsino et al. 2014, 2016). Life form variation is considerable in these centropogonids (see Fig. 1 in Lagomarsino 2016), and increases in diversification rates are also associated with the evolution of fleshy fruit and bat and hummingbird pollination while cooling global temperatures may have affected extinction rates - all, in all, a remarkable radiation (Lagomarsino et al. 2016).
Lobelioideae also make up the largest plant radiation on the Hawaiian islands. Givnish et al. (2006a, 2009a; see also Givnish 1999; 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 (see Shaw & Gillespie 2016 for the progression rule). Species vary in growth habit from trees to herbs, and in leaf morphology, and some species are spiny; herbivory by the now-extinct moa-nalo, a flightless duck as large as a small turkey, is suspected as having driven the evolution of some of this variation. Fleshy fruits have evolved more than once, and there are a number of endemic Hawaiian birds that are/were (some have recently become extinct) pollinators and fruit dispersers (Carlquist 1970; Givnish et al. 1995).
The various chromosomal rearrangements studied by Knox (2014 and references) need to be integrated with the tree once its topology has settled down.
Pollination Biology & Seed Dispersal. For the evolution of the secondary pollen presentation devices in the family, see Erbar and Leins (1988b) and Leins and Erbar (especially 2003a [Cyphia], 2003b, 2005 [Cyphia], 2006, 2010). However, sampling (esp. Cyphocarpoideae and Nemacladoideae) is still incomplete, and understanding the evolution of these mechanisms also awaits a better supported phylogeny, although progress along this front is being made, the individually-varying characters involved in the various secondary pollination devices then being placed on the tree (Crowl et al. 2016). The protandrous flowers are polysymmetric in bud and the introrse anthers are more or less connivent when they dehisce, pollen then being in a position suitable for secondary pollination, whether entangled with the filament hairs or held immediately above the stigmatic head (e.g. Leins & Erbar 2003b, 2010).
Campanuloideae have brush pollination. 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. In Petromarula the stigmatic head is swollen and hairs occur only there (Igersheim 1993a), but otherwise pollination is similar. Phyteuma has coherent corolla lobes although the corolla is open laterally; the style hairs are only partly retractile. The nectar of some Campanuloideae may be brightly colored and then the filament bases are not persistent; normally they are, and they enclose the nectar. Insect pollination is prevalent, but bird (and lizard) pollination is also known, especially in taxa that grow on islands (Olesen et al. 2012).
In Lobelioideae the pollen is retained in a tube formed by the connate anthers; it is forced out by the elongation of the style before the stigmatic lobes separate, recurve, and finally become receptive. 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), although the figure in Fleming et al. (2009) is only 20, while L. Lagomarsino (pers. comm.) estimates about 180 species. Extrafloral nectaries are found in Andean "Centropogon" on the outside of the inferior ovary. These occur mostly in species growing at lower altitudes where ants are to be found, and generalist humming birds are usually the visitors to the flowers (there does not seem to be a connection between these nectaries and pollinators); 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 (Stein 1992). Lobelioideae have 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 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 Clermontia have petaloid sepals, a feature that may have been lost twice (Givnish et al. 2013).
Within Andean Lobelioideae there has been extensive switching betweem fleshy and dry fruits, the result being that Siphocampylus (defined as having capsules) and Centropogon (berries) have turned out to be poly/paraphyletic (Lagomarsino et al. 2014).
Genes & Genomes. The base chromosome number of Lobelioideae is probably 9 (Lammers 1993; Crowl et al. 2016; c.f. Stace & James 1996), in line with that for Asterales as a whole (Bremer et al. 2001). There have been a number of genome duplications in the family, but there seems to be no evidence for an ancestral duplication (Crowl et al. 2016). Genome duplications cannot be linked to the changes in floral symmetry described above (Crowl et al. 2016).
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), Haberle et al. (2008a). The chloroplast gene accD (= ORF512, zpfA) has been lost (Doyle et al. 1995 and references; see also Knox 2014; Rousseau-Gueutin et al. 2013). All told, over 125 inversions, most sizable, are known, and Knox (2014) has pieced together the sequence in which some of the larger inversions occurred. Along with these inversions, protein-coding genes, probably from the nucleus, have moved into the chloroplast (Knox 2014). Biparental transmission of plastids has been recorded (Corriveau & Coleman 1988).
Chemistry, Morphology, etc. Details of the major variation patterns in secondary metabolites within the clade need to be established. Carlquist (1969b) examined the wood anatomy of some Lobelioideae, he noted the very long vessels (with scalariform pitting of the lateral walls; also other characters) of some taxa that grew in very wet habitats; he suggested that paedomorphosis was the cause. Schweingruber et al. (2014) found parallelism in characters of wood anatomy in Campanuloideae, tall species, and species growing in the Arctic, tending to have similar anatomical traits.
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). Some species of Cyphia have a long corolla tube, but the two abaxial petals have slits at their bases; when the flowers are strongly bilabiate, the two abaxial petals are free (Thulin 1978). In Nemacladus (Nemacladoideae) there are sometimes groups of remarkable almost hand-like (in some S.E.M.s) ?nectaries at the bases of two adaxial filaments. It is not known if the style hairs there are retractile. Ostrowskia (Campanuloideae) has anthers with placentoids and the integument is massive (Kamelina & Zhinkina 1998).
Some species of Wahlenbergia have an almost superior ovary. Kausik and Subramanyam (1945, 1947), Rosén (1932, 1949) and Subramanyam (1949, 1970) discuss endosperm development; there may be taxonomically interesting variation in the number of cells that make up the chalazal endosperm haustorium.
For general information on the subfamilies see Schönland (1889), Wimmer (1968), Shulkina et al. (2003) and Lammers (1998 and especially 2006), for stem-node anatomy of Campanuloideae, see Col (1904), for wood anatomy of Campanuloideae, see Schweingruber et al. (2014: esp. the root collar, the transition between the radicle/primary root and the hypocotyl/stem), for inflorescence morphology, see Bull-Hereñu and Claßen-Bockhoff (2011b), for flowers of Downingia, see Kaplan (1969 and references), for pollen see Dunbar (1975a, b), Eddie et al. (2010) and Hong and Pan (2012), also Erbar (2014) for nectaries, Vogel (1998c), Shamrov and Zhinkina (1994) and Shamrov (1998) for ovules, Kolakovsky (1985) for fruit morphology, and Murata (1995), Buss et al. (2001), Cupido et al. (2011 and references) and Koutsovoulou et al. (2013) for seeds, seed coat anatomy/morphology and germination; for the protein bodies in the nuclei, see Bigazzi (1986) and Haberle (1998), and for the remarkable Nemacladus, see Morin and Ayers (2011).
Phylogeny. The relationships of the four major groupings in Campanulaceae have been uncertain for quite some time. Both the monophyly and the relationships of the poorly known Cyphiaceae (there are three subgroups) have been unclear (Lammers 1992), although they are certainly all part of a monophyletic Campanulaceae s. l. (see Cosner et al. 1994; Gustafsson & Bremer 1995; Gustafsson 1996b; Gustafsson et al. 1996). ITS sequence data suggested that one of these groups, Cyphocarpus, was 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 and Nemacladoideae (another subgroup of the old Cyphiaceae). The tree presented by Haberle (1998) suggests the groupings [[Nemacladoideae + Campanuloideae] [Cyphioideae + Lobelioideae]] (Cyphia is the third subgroup), which may 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 (see also Crowl et al. 2016). Lundberg and Bremer (2003) found what was basically a trichotomy of Cyphia, Lobelioideae, and Campanuloideae. Tank and Donoghue (2010) suggested that Cyphia was sister to Campanuloideae and Pseudonemacladus to Lobelioideae; consistent with these relationships is the [[Cyphia + Campanuloideae] clade found by Knox (2014). Indeed, this latter clade seems quite well established, and it is sister to a [Nemacladoideae, Cyphocarpoideae, Lobelioideae] clade - relationships unclear here, although Cyphocarpoideea and Nemacladoideae may be sister taxa - in the extensive (13 loci, 921 taxa) study of Crowl et al. (2016).
General relationships within Campanuloideae are discussed by Eddie et al. (2002, 2003), Cosner et al. (2004), and Olesen et al. (2012). Platycodon, Codonopsis and Cyananthus form a clade and are strongly supported as being sister to all other Campanuloideae (e.g. Cosner et al. 2004; Crowl et al. 2014; Hong & Wang 2015). However, relationships in the rest of the family are not so clear. Both Campanula and Wahlenbergia are seriously polyphyletic. Most of Wahlenbergia and some other genera form a clade sister to the rest of the subfamily, while within the latter, W. hederacea (now = Hesperocodon hederacea), linked 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; Crowl et al. 2014). Other studies placed with Wahlenbergia and other immediate relatives (Mansion et al. 2012; Hong & Wang 2015). The Campanula clade was divided into two main clades, one centred on Campanula s. str. and the other on Rapunculus, while successively basal to these (the relative order is unclear) are the Jasione (mentioned already) and Musschia clades, the latter also including some species of Campanula (e.g. Cupido et al. 2013; Crowl et al. 2014). Relationships were rather different in the four chloroplast gene analysis of Hong and Wang (2015), where Jasione and Musschia were successively sister at the base of the Campanula group. Although support was rather strong, sampling was good only in the Platycodon group, while in Crowl et al. (2014) sampling was extensive, but largely in the Campanula group. Indeed, Mansion et al. 2012) carried out a particularly extensive study in Campanuleae analysing variation in the petD gene for 3/4 (310/420 species) of all Campanula, plus related taxa and some other Campanulaceae. Within Campanuleae, they found the relationships [[some Campanula + Musschia] [[Feeria + Jasione] + The Rest]] - all told, there were 17 clades with species of Campanula, and in five of these they were mixed with representatives of other Campanuleae genera (Mansion et al. 2012).
Within Lobelioideae, molecular data show that Lobelia is wildly paraphyletic, all other genera of the subfamily being emmbedded within it (Knox & Muasya 2001; Antonelli 2008, 2009; Knox et al. 2008; Lagomarsino et al. 2014; L.-Y. Chen et al. 2016). Reading up the tree is dizzying both in terms of the names and the geography of the clades. Within South American lobelioids, Centropogon and Siphonocampylus, for example, are not monophyletic (e.g. Lagomarsino et al. 2011, 2014), but there is fair support for many relationships in the whole "Siphocampylus"-Burmeistera-"Centropogon"-Lysipomia clade. Within Burmeistera classical sectional limits break down, and although resolution still leaves something to be desired, geograhically- and morphologically-circumscribed clades are becoming evident (Uribe-Convers et al. 2016b).
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). I follow Hong and Wang (2015) for a tribal classification of Campanuloideae, although it is quite possibly premature to do this.
Generic limits need much attention, Campanula, Lobelia, and Wahlenbergia and relatives all being particular problems (see also Kilian in Kadereit et al. 2016). A much more broadly delimited Campanula might be a reasonable solution to its extensive paraphyly, and its segregate genera have been 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) and Q. Wang et al. (2014) suggest the generic pulverization of the Codonopsis area. The current classification of Lobelioideae is almost no use whatsoever, and considerable expansion of Lobelia may be a course to take. Thus the monophyletic Burmeistera is embedded in a clade where Siphocampylus and Centropogon are hopelessly intermingled (most of the infrageneric groups are also para/polyphyletic), the whole being a clade coming from within a paraphyletic Lobelia (Lagomarsino et al. 2014; L.-Y. Chen et al. 2016), and the sectional classification of Lobelia (Lammers 2011) necessarily needs a complete overhaul.
Previous Relationships. Takhtajan (1997) divided Campanulaceae s.l. into four families; these, plus Pentaphragmataceae and Sphenocleaceae (for the latter, see Solanales), made up his Campanulanae. Cronquist (1989) had taken the opposite tack, recognizing a broadly circumscribed Campanulaceae that included the four families just mentioned, plus some other families that are elsewhere in Asterales, in his Campanulales.
Botanical Trivia. At less than 5.5. mm tall, sometimes lacking true leaves and flowering from the axils of its cotyledons, Lysipomia mitsyae is one of the world's smallest eudicots (Sylvester et al. 2016).
Thanks. I am grateful to Tatyana Shulkina and Laura Lagomarsino for helpful discussions.
[Pentaphragmataceae [[Alseuosmiaceae [Phellinaceae + Argophyllaceae]] [Stylidiaceae [Menyanthaceae [Goodeniaceae [Calyceraceae + Asteraceae]]]]]]: (corolla lobes with marginal wings) [could go here].
Age. An age for this node is (91-)78(-68) m.y. (Wikström et al. 2015) or ca 84 m.y. (Tank et al. 2015: Table S1, S2).
PENTAPHRAGMATACEAE J. Agardh, nom. cons. Back to Asterales
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, gynoecial nectaries in cavities so formed; 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; endosperm starchy, chalazal haustorium 0, embryo medium-short (1/3rd); 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 (Kapil & Vijayaraghavan 1965).
For general information, see Lammers (2006), for wood anatomy, see Carlquist (1997b), for the nectary, see Vogel (1998c), and for pollen, see Dunbar (1978).
[[Alseuosmiaceae [Phellinaceae + Argophyllaceae]] [Stylidiaceae [Menyanthaceae [Goodeniaceae [Calyceraceae + Asteraceae]]]]]: C connate; ovary inferior [?level].
Age. Estimates of the age of this node (but note topology) are (79-)73, 67(-58) m.y. (Bell et al. 2010), (88-)84, 76(-72) m.y. (Wikström et al. 2001) and (84-)73(-62) m.y. (Wikström et al. 2015).
[Alseuosmiaceae [Phellinaceae + Argophyllaceae]]: plant woody; lamina gland-toothed; x = 8.
Age. An estimate of the age of this node (note topologies again!) is (71-)61, 56(-44) m.y. (Bell et al. 2010), (73-)69, 66(-62) m.y. (Wikström et al. 2001), ca 71.9 m.y. (Magallón et al. 2015) or ca 74 m.y. (Tank et al. 2015: Table S1, S2).
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); Wikström et al. (2015) suggested a grouping [Argophyllaceae [Phellinaceae + Alseuosmiaceae]], but with little support.
ALSEUOSMIACEAE Airy Shaw Back to Asterales
± Woody; condensed and ellagitannins +, inulin?, iridoids 0; young stem with separate bundles; true tracheids +; rays narrow to broad (wood rayless - Alseuosmia); 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 (hardly - Platyspermation), (wings fringed; erose); 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. Ecology & Physiology. In New Zealand Alseuosmia pusilla appears to mimic (Batesian mimicry) the leaves of Pseudowintera colorata - it has sequiterpene dialdehydes and tastes rather nasty, as do other Winteraceae (Yager et al. 2016). See also Boquila trifoliata (Ranunculales-Lardizabalaceae) and Loranthaceae for possible mimicry.
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 the stem has 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 Gregory (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 separation of these two families are (68-)63, 62(-57) m.y.a. (Wikström et al. 2001).
PHELLINACEAE Takhtajan Back to Asterales
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 were in his Celastrales.
ARGOPHYLLACEAE Takhtajan Back to Asterales
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: as Escalloniaceae) 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]]]]: fructan sugars accumulated as isokestose oligosaccharides [inulins].
Age. The age of this node is around 76.5 m.y. (see Magallón et al. 2015), (82-)71(-61) m.y. (Wikström et al. 2015) or ca 78 m.y. (Tank et al. 2015: Table S1, S2).
Evolution: Divergence & Distribution. Exactly where acquisition of monosymmetry is to be placed within Asterales is unclear; monosymmetric and polysymmetric clades more or less alternate in this part of the tree.
STYLIDIACEAE R. Brown, nom. cons. Back to Asterales
Young stem with separate bundles; nodes 1:1; lamina 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).
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 (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
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 only towards the inside [xylem only], interxylary phloem +; wood rayless [?always]; vessel elements with simple perforation plates; hairs glandular; leaves pseudoverticillate or in rosettes, with axillary hairs; flowers resupinate [median sepal abaxial], (split-monosymmetric); K (6), connate, 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  (adaxial much reduced), placentation free-central, stigma small, dry; fruit dahiscing laterally from the apex, 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, 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.]
Age. Diversification in Stylidioideae has been dated to ca 39 m.y.a. (Wagstaff & Wege 2002).
Evolution: 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 the 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 in both corolla tube and column lengths; even the pollen varied in colour. However, as the column of Stylidium hits the pollinator, it adjusts to its body surface, so placing pollen in a place that allows the insect to be an effective pollinator (Armbruster 2014); as Armbruster notes, the flower is "phenotypically specialized to be an excellent ecological generalist" (ibid.: p. 7).
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, although 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, 2013). In older stems of Donatia the cortex is very thick, and the vascular tissue forms a narrow cylinder in the center (Chandler 1911).
The fertile stamens are the adaxial pair. Carolin (1960b) drew the anthers of Donatia as being introrse. 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 a single abaxial (adaxial in the text) 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 (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 (1969a), 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 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, in a rbcL + ndhF analysis it was grouped with Levenhookia, but both positions had 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]]]: herbs; fructans, caffeic acid +; cauline stele with separate vascular bundles; 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 grains bicellular; nectary +; G , stylar bundles branched, stigma papillate; integument >10 cells thick, antiraphal vascular bundle proceeding to the micropyle; endosperm haustoria 0, embryo long; x = 9.
Age. Estimates of the age of this node vary - (71-)63, 58(-48) m.y. (Bell et al. 2010), ca 68.3 m.y. (Magallón et al. 2015), (73-)69, 65(-61) (Wikström et al. 2001), 72.2 or 73.7 m.y. (Tank et al. 2015: Table S1, S2), (135-)82.5(-66) m.y.a. (Jabaily et al. 2014, q.v. for other dates, some older) and (76-)65(-56) m.y. (Wikström et al. 2015). Barreda et al. (2015) offer a series of estimates, at (103.3-)96.5, 69.1(-65.4) m.y.a. they are mostly older, while (95.8-)84.5(-71.6) m.y. is the estimate in Panero and Crozier (2016: Table S1).
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).
The separate vascular bundles in the stem may be connected with the herbaceous habit that is so common here. 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). Presence of sclereids and multi-nucleate tapetal cells may be additional synapomorphies (Lundberg 2009, q.v. there and Katinas et al. 2016 for more possible synapomorphies).
Chemistry, Morphology, etc. The androecium has spiral initiation in some Menyanthaceae, Asteraceae and Goodeniaceae - and also Araliaceae (Erbar 1997). For inflorescence morphology and evolution, see Pozner et al. (2012).
MENYANTHACEAE Dumortier, nom. cons. Back to Asterales
Aquatic or marsh herbs; flavonols only +, little oxalate accumulation, tannin 0; cork?; vascular cambium 0[?]; vascular bundles often scattered; nodes 3:3, 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; (oppositipetalous fringed scales +); anthers sagittate; tapetal cells with fused nuclei; pollen grains (three-celled), ± oblate or ± prolate, (syncolporate; isolated triangular polar areas), surface striate, etc.; G ± superior, placentation parietal, style (0), with 2-several vascular bundles, stigma bilobed-spathulate, wet; funicle vascularized, 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; chloroplast rpl2 intron 0.
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)?
Genes & Genomes. For the missing chloroplast rpl2 intron, see Downie et al. (1991b).
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).
Eichler (1878) drew the flower of Menyanthes with an oblique plane of symmetry. 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 general information, see G. Kadereit (2006), for floral development, see Erbar (1997), for pollen, see Nilsson (1973), for embryology, see Stolt (1921) and Maheswari Devi (1963), and for seed morphology, see Chuang and Ornduff (1992).
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 (see also Du & Wang 2014; Du et al. 2016) while Villarsia is very much paraphyletic. Many relationships within Nymphoides are as yet poorly supported; whether or not the flowers are heterostylous seems a very labile character (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). 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 tectum microperforate, columellae bifurcating; stigma dry, papillae all similar, involved in both pollen presentation and reception; K persistent in fruit.
Age. Kim et al. (2005) date this node to (80-)64.5(-49) m.y.a., Tank et al. (2015: Table S1, S2) to around 59.8 or 56.1 m.y., Magallón et al. (2015) to about 57 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 (50-)44, 40(-30) m.y., Xue et al. (2012) to only 39.7-39.0 m.y., and Wikström et al. (2015) to (63-)55(-49) m.y., although other recent estimates are much older, some (120-)78(-62) m.y.a. to (130-)113(-66) m.y.a. (Jabaily et al. 2014), ca 96.7 m.y. (Denham et al. 2016) or (86.9-)75.2(-63.6) m.y.a. (Panero & Crozier 2016).
Evolution: Divergence & Distribution. Although secondary pollen presentation occurs throughout this clade, there is considerable variation in the details of how it is done (Leins & Erbar 2003b, 2006 and references), so it is debatable whethher or not it should be an apomorphy (see also Katinas et al. 2016).
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).
GOODENIACEAE R. Brown, nom. cons. Back to Asterales
Herbs (woody, arborescent); O-methyl flavonols only, alkaloids +; cork also cortical; (vessel elements with scalariform perforation plates); (medullary vascular bundles +); nodes 1:1 (3:3, 5:5); branched sclereids +; indumentum variable, hairs often minutely warty; lamina margins entire to toothed; flowers split-monosymmetric; C induplicate-valvate, lobes with marginal wings; A basifixed; pollen mesocolpia concave; nectary usu. 0; G also , (placentation ± basal), style curved, vascular bundles 3-4, branching apical, branches divergent ["broccoli-like"], apical hairy pollen-collecting indusium and stylar cup +, stigma initially included, bilobed; integument 6-20 cells across, hypostase +; synergids long, hooked, antipodal cells persistent; fruit dehiscing laterally, septicidal (and loculicidal); testa 7-14 cells thick, usu. with vascular bundle ± encircling seed, exotestal cells usu. palisade (crystalliferous), all walls (especially inner) thickened, (hypodermal layers lignified); endosperm well developed; n = 9; rpl16 intron missing.
12[list]/430. Very largely Australian, Scaevola alone pantropical (map: esp. Leenhouts 1957b, excluding Scaevola).
Age. One age of crown-group Goodeniaceae is estimated at (90-)67.3(-53) m.y.a. (Jabaily et al. 2014).
1. Dampiera, etc.
Anthers connate; (pollen in tetrads, surface perforate-reticulate), (surface rugulate); stigma not protruding past the indusium.
Age. The crown-group age of this clade is around (76-)59.2(-44) m.y.a. (Jabaily et al. 2014).
3/97: Dampiera (66), Lechenaultia (20). Australia (S. New Guinea).
[Brunonieae + Goodenieae]: pollen microspinulose, spines acute, endapertures with distinct borders; stigma protruding past the indusium.
Age. The age of this node is (68-)52.1(-40) m.y.a. (Jabaily et al. 2014).
2. Brunonieae G. Don
Herbs; inflorescence capitate, involucrate; K with filamentous hairs, C ± polysymmetric, lobes lacking marginal wings; G superior, stylar hairs forming brush; ovule single, basal, erect; fruit indehiscent, achene/nut; testa thin-walled, compressed; endosperm 0, cotyledons massive.
1/1: Brunonia australis. Throughout Australia.
Synonymy: Brunoniaceae Dumortier, nom. cons.
3. Goodenieae Dumortier / core Goodeniaceae
Herbs, annual to perennial, to shrubs; (C spurred), (lobes lacking marginal wings); A adnate to base of C; (G superior); (fruit a drupe), (capsule - Velleia); (seeds winged); (anticlinal exotestal walls sinuous); 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.]
Age. The age of crown-group Goodenieae is estimated to be (48-)37.1(-27) m.y.a. (Jabaily et al. 2014).
Synonymy: Scaevolaceae Lindley
Evolution: Divergence & Distribution. For records of fossil pollen, see Barreda et al. (2010a).
Jabaily et al. (2014) discuss ideas about the origin (place equivocal) and time (quite a spread of ages) for the origin of Goodeniaceae. 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; the pollen of Brunonia, with its capitate inflorescence and flowers with straight styles, is held in a brush formed by stylar hairs.
The seeds of many Goodenieae in particular are myrmecochorous (Lengyel et al. 2009, 2010), others have circumferential wings that are mucilaginous when wetted (Jabaily et al. 2012).
Genes & Genomes. The mitochondrial genes cox1, atp1 and matR showed massive divergence (Barkman et al. 2007: Scaevola only sampled).
Chemistry, Morphology, etc. The cortical bundles in the stem sometimes reported for the family are leaf traces.
For a morphometric analysis of corolla shape in core Goodeniaceae, see Gardner et al. (2016); slit-monosymmetric fan flowers are rather distinct from other other corolla "types". The lateral veins of the corolla of Brunonia unite in the receptacle (Erbar 1997).
See also Carolin (1978, 2006) for general variation and morphology, Gustaffson et al. (1997) for pollen morphology, Subramanyam (1950a) for embryology, Carolin (1966) for seeds and fruits, 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, one includes Lechenaultia and allies, and the other Scaevola, a paraphyletic Goodenia, and allies. Within the latter clade Brunonia is sister to the rest, and Gardner et al. (2015), using genome skimming (some conflict between relationships suggested by nuclear and those by chloroplast genes) found a strongly supported set of relationship in which Scaevola s.l. was sister to the rest, and Goodenia was paraphyletic.
Classification. For a general account of most of the family, see Fl. Austral. vol. 35 (1992). Generic limits around Goodenia are difficult and the limits of the genus may have to be severely circumscribed (Jabaily et al. 2012; Gardner et al. 2015). Most of the numerous features in which Brunonia differs from other Goodeniaceae are autapomorphies (see above). Some of these features might seem to suggest relationships with Asteraceae (Gustafsson 1996a), but clearly the exclusion of Brunonia from Coodeniaceae, as by Cronquist (1981), makes Goodeniaceae paraphyletic (Jabaily et al. 2012).
Thanks. I am grateful to Mats Gustafsson for comments.
[Calyceraceae + Asteraceae]: inflorescence capitate, involucrate, with cymose units; flowers sessile, rather small, polysymmetric; C tubular, deeply lobed, commissural veins connate; filament collar +; pollen prolate, shape of colpus end equivocal, spines blunt, columellae [in endosexine] evenly spaced, internal foraminae, caveae, internal tectum 0, foot layer continuous, pollenkitt +; stylar vascular bundles branching near apex, branches parallel, pollen presented on stigma; ovule single [per flower]; fruit a cypsela, K persistent, modified, involved in dispersal; genome duplication [palaeotetraploidy]; x = 8/9.
Age. These two clades diverged an estimated (49-)45.5(-42) m.y.a. (K.-J. Kim et al. 2005), ca 48.8 m.y. (Tank et al. 2015: Table S1, S2), ca 49.3 m.y.a. (Magallón et al. 2015), ca 51 m.y.a. (Bremer et al. 2004), (56-)49(-47) m.y.a. (Wikström et al. 2015), (61-)54.4(-49) m.y.a. or older (Jabaily et al. 2014), or as much as (80.1-)69.5(-59) m.y.a. (Panero & Crozier 2016), ca 76.5 m.y. in Denham et al. (2016) and ca 74 m.y. (C.-H. Huang et al. 2016) - or only ca 55 m.y. in the latter.
Evolution: Divergence & Distribution. Asteraceae-Barnadesioideae and -Fatimimananthoideae, the two basal clades in Asteraceae, and Calyceraceae are South American, and this whole clade may have originated there, indeed, the six basal clades in Asteraceae are all largely South American.
Katinas et al. (2016) discussed possible atylar apomorphies in Calyceraceae and Asteraceae, particularly Barnadesioideae, in some detail, and many of their suggestions are adopted here. 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). Indeed, 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, similarly, 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. I have placed several pollen characters at this node to help in interpreting the changes in pollen morphology within Asteraceae as detailed by Blackmore et al. (2009). The inflorescences of the two families can be interpreted as being fundamentally similar, despite the largely indeterminate construction of the asteraceous capitulum (see below).
Genes & Genomes. For a palaeotetraploidy event that can be placed at this node, see M. S. Barker et al. (2016a) and C.-H. Huang et al. (2016). For possible base numbers for this clade, see Denham et al. (2016).
Understanding more about the expression of CYC (Cycloidea) genes in this clade - and indeed in Asterales as a whole - is likely to be interesting. Chapman et al. (2012) note that Acicarpha (Calyceraceae) has only CYC2a, genes, Dasyphyllum (Barnadesioideae, flowers polysymmetric again) also has CYC2c genes, while the other Asteraceae studied all had CYC2b, d and e genes as well. Members of the CYC2c gene family are involved in the monosymmetric phenotype in which corolla formation on the adaxial side of the flower is more or less reduced (see also Garcês et al. 2016).
Chemistry, Morphology, etc. Calyceraceae and Barnadesioideae have a similar simple flavonoid profile.
The distinctive capitulum of Asteraceae lacks a terminal flower and seems to be basically racemose, unlike that of its sister taxon, Calyceraceae. However, it can be derived from the inflorescence of the latter with its cymose lateral branches if these latter are suppressed (e.g. Pozner et al. 2012). Claβen-Bockhoff and Bull-Hereñu (2013) suggest that the capitulum develops centripetally by apical fractionation, although they note that in supercapitulae (capitulae of capitulae) the development of the whole inflorescence may be centrifugal - as may be the development of these ray flowers. Thus in Gorteria the outermost (ray) flowers develop 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 (see also Pozner et al. 2012; Denham et al. 2016 for phylogeny og Calyceraceae), although the development of the capitulum of Gerbera, in the more basal Mutisioideae, and the role that the LFY gene plays in both inflorescence and floral development is compatible with the interpretation that ray flowers correspond to these lateral branches of the inflorescence of Calyceraceae (Zhao et al. 2016; see also Bello et al. 2013: Anacyclus).
Previous Relationships. Both Cronquist (1981) and Takhtajan (1997) placed the two families in separate, if adjacent, orders.
CALYCERACEAE Richard, nom. cons. Back to Asterales
Herbs; ?flavonols 0; cork?; nodes ?; pericyclic fibres 0; plant ± glabrous; lamina margins entire; inflorescence entirely made up of cymose units, (not always obvious, but a terminal flower - Acicarpha), flowering ± centrifugal, heads homogamous; all flowers bracteate, polysymmetric; 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 grains with intercolpar depressions, (spines 0); (G embedded in inflorescence axis), stigma capitate (slightly bilobed); 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) or (40-)22(-7) m.y.a. (Wikström et al. 2015); (57-)39.2(-24.9) m.y. are the estimates in Panero and Crozier (2016).
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!
Phylogeny. There are two main clades in the family, and details of relationships within those clades depend in part on whether nuclear ITS or chloroplast data are examined; Boopsis in particular is hopelessly polyphyletic, and the only possibly monophyletic genus is Acicarpa (Denham et al. 2016).
Synonymy: Boopidaceae Cassini
ASTERACEAE Berchtold & J. Presl, nom. cons. // COMPOSITAE Giseke, nom. cons. et nom. alt. Back to Asterales
(Plant ± shrubby); iso/chlorogenic acid, isoflavonoids, pentacyclic triterpene alcohols, terpenoid essential oils, (various alkaloids), a variety of fatty acids in the seeds, tannins, iridoids 0; (vascular tissue in 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 +; lamina vernation often conduplicate or revolute, margins various; capitulum with phyllaries in several series, lacking a terminal flower, cymose construction obvious in the area of the ray flowers; receptacle scrobiculate, bracts/bracteoles 0; (heads heterogamous, gynomonoecy common), (some flowers [esp. ray flowers] monosymmetric); K reduced, C midveins 0 (+), commissural veins connate at apex of lobes, lobes of disc corollas usu. longer than wide; anthers connate, apical connective conspicuous, basally calcarate [sagittate], caudate [theca with basal appendage], (laciniate), endothecial cells elongated parallel to main axis of anther [?level]; tapetum amoeboid (glandular); pollen grains tricellular [?level], 37-49.1 µm in diam., exine 6.1-6.7 µm across; nectary annular; style arms [branches, lobes] short [<1.4 mm long], stigmatic surface continuous, papillae with a single function [pollen presentation or reception]; ovule basal, epitropous, integument (4-)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), (± obliterated), exotestal cells thickened on anticlinal and/or inner periclinal walls, undistinguished; endosperm scanty to 0, (nuclear); x = 27; protein bodies in nuclei; sporophytic incompatibility system present.
1620[list]/25,040 - thirteen groups below. World-wide (map: Vester 1940; Hultén 1971). [Photo - Flowers, and more Flowers.]
Age. Crown-group Asteraceae are 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., ages in Swenson et al. (2012) range mostly from (71.1-)52.6, 47.4(-45.4) m.y., in Panero and Crozier (2016) are as much as (74.4-)64.7(-55.1) m.y. (see also Jabaily et al. 2014 for similar estimates) and in C.-H. Huang et al. (2016) are ca 72.1 m.y. (or only (53-)52.5(-52) m.y.), while ca 61.4 m.y. is the age in Denham et al. (2016) and 47.6-47.3 m.y in Funk et cl. (2014). (Heads  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].)
Samant and Mohabey (2014) think that the Late Cretaceous palynomorph Compositopollenites from India is evidence that the family was around at this early date. Analysis of pollen from Antarctica dated 76-66 m.y.o. suggests that it was from a barnadesiaceous plant, and a crown age for Asteraceae of around (91.5-)85.9(-82.4) m.y. was suggested (Barreda et al. 2015: fig. 5, suppl.; see also discussion in Proc. National Acad. Sci. U. S. A. 113: E 411, 412. 2016.), although other estimates, at (76.4-)67.9, 55.8(-53.6) m.y., are somewhat younger (Barreda et al. 2015: suppl.).
1. Barnadesioideae Bremer & Jansen
Notably poor in flavonoids, flavones 0; paired axillary thorns/spines + (0); hairs tricellular [pedicel cell (= "golf-tee cell") + ± globose cell + elongated cell - throughout plant]; (receptacle hairy); (flowers ± monosymmetric, esp. 4:1, etc.); corolla hairy, (commissural veins not connate at apex of lobes); anther with apical connective rounded to bifid, (not calcarate), (not caudate); pollen (lophate), (with intercolpar depressions), (± caveate), foot layer discontinuous, exine columellate-granulate [columellae sinuous]; style (strongly curved - Fucaldea stuessyi), arms rounded to cuneate, abaxially (minutely) rounded-papillate (smooth), vascular bundles at most entering base of arms; secondary pollen presentation pump/deposition/brush types; cypselas ?-ribbed, villous, foxy coloured, pappus uniseriate, various; n = 8, 12, 24-27.
9/92. South America, esp. Andean (map: red, see Karis et al. 1992; Ezcurra 2002; Funk & Roque 2011). [Photo - Flower.]
Age. The age of crown-group Barnadesioideae is about 39.4-19.4 m.y. (Funk et al. 2014: Dussenia), (48.7-)33.7(-23.6) m.y. (Panero & Crozier 2016: Table S1) or (48.8-)37.4(-25.6) m.y. (Abrahamczyk et al. 2017).
[Famatinanthoideae [Mutisioideae [Stifftioideae [Wunderlichioideae [Gochnatioideae [Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]]]]]]: anther base lignified; internal tectum +, homogeneous [?level]; secondary pollen presentation brush-type; stylar vascular bundles entering stigmatic arms (unbranched), stigmatic/stylar papillae with different shapes [for pollen presentation and reception]; pappus 2-5-seriate; 22.8 kb chloroplast DNA inversion, 3.3 kb inversion nested within it.
Age. The age of this node is around (66.5-)58.8(-51.4) m.y. (Panero & Crozier 2016: Table S1).
2. Famatinanthoideae S. E. Freire, Ariza & Panero
Cork deep-seated; stomata raised, with sub-stomatal cavity; leaves opposite, amphistomatal; phyllaries 3-seriate; ray florets bilabiate [2:3], disc florets deeply lobed [ca 1/2]; anther with apical connective long, apiculate, sclerified; pollen surface microechinate/rugulate; style arms abaxially with groups of large cells [cobblestone-like], apex cuneate; pappus 2-3-seriate, of dimorphic barbellate bristles; n = 27.
1/1: Famatinanthus decussatus. N.W. Argentina (map: see above, green).
[Mutisioideae [Stifftioideae [Wunderlichioideae [Gochnatioideae [Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]]]]]: often herbaceous; (benzofurans + [benzene + furan - C4H40 (heterocyclic) rings]); leaves usu. triplinerved; corolla lobing?, commissural vein fusion?; style arms long [?definition]; cypselaa with twin hairs [unicellular to uniseriate base, apical cell un/equally 2-armed], pappus capillary, developing late: ?genome duplication.
Age. The age of this node is about (62.7-)55.9(-49.2) m.y. (Panero & Crozier 2016: Table S1) orsomewhere aroubnd 61.5 to 47.5 m.y. (C.-H. Huang et al. 2016: three estimates).
Panero et al. (2014) suggested that the macrofossil, Raiguenrayun cura, a capitulum from the Middle Eocene of Patagonia ca 47.7 m.y.a., and its associated pollen (Barreda et al. 2010b, 2012a), is assignable to this node.
3. Mutisioideae Lindley
Capitulae variously aggregated); (receptacle hairy); (heads heterogamous), (central flowers subligulate, etc.), (deeply lobed [1/3-1/2],) (lobing 4:1, 3:1); anther with apical connective rounded (acute), rarely calcarate; pollen ?shape, surface microechinate; style arms (short - e.g. Adenocaulinae), apex rounded, truncate, or ± cuneate, abaxially hairs +, unicellular, (at apex only, 0); also deposition/brush-type secondary pollen presentation; cypsela 5- or 10-ribbed, hairy to glabrous, (pappus uniseriate), (2-many-seriate, of dimorphic barbellate bristles; n = (6-)9(+); (genome duplication).
46/637: Acourtia (65), Chaptalia (60), Mutisia (50), Trixis (50), Gerbera (35). South America (North America, East Asia).
Age. The age of crown-group Mutisioideae is estimated to be (61.3-)52.5(-43.4) m.y. (Panero & Crozier 2016: Table S1).
Synonymy: Mutisiaceae Burnett, Nassauviaceae Burmeister, Perdiciaceae Link, nom. inval.
[Stifftioideae [Wunderlichioideae [Gochnatioideae [Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]]]]: (leaves opposite); style arms ± rounded at the apex; x = ?
Age. This node can be dated to (69.1-)55.3(-48.6) m.y.a. (Panero & Crozier 2016: Table S1).
4. Stifftioideae Panero
(Marginal, central flowers ± monosymmetric); (C lobes long, ± coiled); apex of anther appendage ± acute; pollen spherical, surface echinate or not; style arms abaxially glabrous, (surface bullate); deposition/brush-type secondary pollen presentation quite common; cypsela 10-ribbed, glabrous; n = .
Ca 10/35. Venzuelan-Guianan (Andes, N.E. South America).
Age. Crown-group Stifftioideae - [Stifftia + The Rest]- can be dated to (52-)27.4(-7.9) m.y.a. (Panero & Crozier 2016: Table S1).
[Wunderlichioideae [Gochnatioideae [Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]]]: sesquiterpene lactones + [level?].
Age. This node is about (61.2-)54.5(-48.1) m.y. (Panero & Crozier 2016: Table S1).
5. Wunderlichioideae Panero & Funk
(Receptacle alveolate), (paleaceous - Wunderlicheae); (marginal flowers monosymmetric); apex of anther appendage acute to apiculate; pollen (spiny), ?other characters; style arms abaxially with scale-like multiseriate hairs [Wunderlichieae] or glabrous; cypsela 10-ribbed, hairy to glabrous, (pappus paleaceous); n = ?; 6 bp deletion in PEP subunit β rpoB gene.
Ca 8/48. Venzuelan-Guianan (E. South America, S.W. China).
Age. The age of crown-group Wunderlichioideae ([Wunderlichia + Hyalis]) is estimated to be (59.6-)46(-24.4) m.y. (Panero & Crozier 2016: Table S1).
[Gochnatioideae [Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]]: ?
Age. This node is dated to (60.2-)53.6(-47.3) m.y.a. (Panero & Crozier 2016: Table S1).
6. Gochnatioideae Panero & Funk
(Receptacle alveolate); (heads heterogamous); apex of anther appendage ± apiculate; pollen ?shape, anthemoid[!]; style arms abaxially glabrous, adaxially concave; cypsela 5-ribbed, hairy, (pappus uniseriate); n = 22, 23, 27.
8/85: Anastraphia (33). Central and South America, esp. the Caribbean and southern South America.
Age. The age of crown-group Gochnatioideae is 24.9-23 m.y. (Funk et al. 2014) or (54.5-)36.7(-14.2) m.y. (Panero & Crozier 2016: Table S1).
[Hecastocleidoideae [Carduoideae [Pertyoideae [Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]]]]: pollen grains spherical, columellae sausage-like; deletion in PEP subunit β rpoB gene.
Age. The crown age of this clade is some 38-32 m.y. (K.-J. Kim et al. 2005) or (58.1-)51.7(-45.7) m.y. (Panero & Crozier 2016: Table S1).
7. Hecastocleidoideae Panero & Funk
Shrubby; leaves spiny; capitulae 1-flowered, grouped into synflorescence, synflorescence bracts attractive; heads homogamous, all flowers polysymmetric, corolla 5-lobed; apex of anther appendage rounded; pollen tricolpate; style arms abaxially glabrous; cypsela 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?; capitulae variously aggregated, apical capitulum flowers first ["capitulescence cymose"]; carpels of disc flowers [at least] superposed, sweeping hairs +[?]; [?cypsela rib # and indumentum], x = 10; genome duplication [= palaeohexaploidy - ?here], deletion and insertion in PEP subunit β rpoB gene.
Age. This node is about (55.5-)49.8(-44) m.y.o. (Panero & Crozier 2016: Table S1) or between ca 54 and ca 42.5 m.y. (C.-H. Huang et al. 2016: three estimates).
8. Carduoideae Sweet
Plant often herbaceous, biennial habit common; (laticifers +), (resin ducts +); leaves dissected, teeth spine-tipped; flowers polysymmetric (monosymmetric); pollen (psilate), columellae "medium thickness", with internal tectum; ring of hairs below style arms; brush-type secondary pollen presentation common, (flowers touch-sensitive); (cypsela lacking twin hairs), (pappus uniseriate); exotestal cells palisade; n = 9, 12.
83/2,864: Centaurea (695), Cousinia (655), Saussurea (485), 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.; around (45-)30.6(-17.4) m.y. is the age in Panero and Crozier (2016: Table S1, [Oldenburgia + Carthamnus]).
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; style hairy.
Age. The age of this node is around (54-)48.4(-42.9) m.y.a. (Panero & Crozier 2016: Table S1).
9. Pertyoideae Panero & Funk
Herbs to shrubs; flowers not bilabiate, corolla irregularly divided; (pollen with solid spines); style arms short, apices rounded (to acuminate), abaxially pilose to papillose; pappus usu. uniseriate; of (plumose) bristles; n = 12-15.
5-6/70: Ainsliaea (50). Afghanistan to East (and Southeast) Asia.
Age. The age of crown-group Perytoideae is about (38.8-)18.8(-2.6) m.y. (Panero & Crozier 2016: Table S1).
[Gymnarrhenoideae [Cichorioideae [Corymbioideae + Asteroideae]]]: herbaceous habit esp. common; pollen echinate or lophate.
Age. This node is some (52.1-)46.8(-41.7) m.y.o. (Panero & Crozier 2016: Table S1) or somewhere between ca 52 and 41 m.y. (C.-H. Huang et al. 2016: three estimates).
10. Gymnarrhenoideae Panero & Funk
Plant annual or perennial, acaulescent (not), amphicarpic; (heads grouped into synflorescence), of two kinds; anthers lacking apical appendages or with a triangular appendage, ecaudate or with short obtuse ± connate tails; endothecium ± absent; ?pollen caveate, infrategular baculae +; stigmatic surface in two bands [Cavea]; pappus of scales or scabrid; n = 9, 10.
2/2. North Africa to the Middle East, also the Himalayas (Tibet, Sikkim, Szechuan).
[Cichorioideae [Corymbioideae + Asteroideae]]: pollen spines 2-5 μm long; 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), (51.1-)45.9(-40.9) m.y. (Panero & Crozier 2016: Table S1), or somewhere between 50.5 and 40 m.y. (C.-H. Huang et al. 2016: three estimates).
11. Cichorioideae Chevallier
Plants perennial; (latex + - Cichorieae); (phyllaries ± uniseriate); (all flowers ligulate - Lactuceae), (true ray florets +); endothecium ± absent; (pollen caveate), (internal foraminae), (with internal tectum), columellae aggregated under spines; carpels collateral, style arms usu. acute at apex, with long sweeping hairs; brush-type secondary pollen presentation common; n = (7-)9-10(-13).
224/3,994: Vernonia (800-1000, but see below), Crepis (200), Scorzonera (175), Lactuca (125), Lepidaploa (115), Tragopogon (110), Lessinganthus (100), Hieracium (90-1000+), Vernonanthura (65), Hypochaeris (60), Sonchus (60), Taraxacum (60-500+). World-wide.
Age. Crown-group Cichorioideae are (45.4-)36.7(-27.9) m.y.a. (Panero & Crozier 2016: Table S1 [Sonchus + ]).
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, spines pointed.
Age. The age of this clade is about (49.4-)44.4(-39.8) m.y. (Panero & Crozier 2016: Table S1).
12. Corymbioideae Panero & Funk
Plant perennial; sesquiterpene lactones 0, macrolides +; leaves linear, with parallel veins; heads with 1 flower, involucral bracts 2; C with broad, patent lobes; anthers black, apical appendage reduced, shortly sagittate, excaudate; style arm apices variable; pappus of bristles or scales; n = 8.
1/7. South Africa (map: from Weitz 1989).
13. Asteroideae Lindley
(Plants shrubby), (annual); sesquiterpene lactones at biogenetic levels 3 and 4 [sic], (6,8-deoxygenation of flavonoids), benzopyrans, benzofurans, (pyrrolizidine alkaloids - esp. Senecio s.l.), C10 acetylenes + [?level in Asteraceae]; secretory canals 0[?]; (flowers bracteate); often radiate [ray florets [3 lobed], female/sterile], disc florets polysymmetric, perfect, C shallowly lobed; anthers (free), (black), (ecalcarate), ecaudate; pollen 25.0-34.3 µm in diam., colpus ends acute, (spines solid), (internal foramina 0), exine 2.3-4.2 µm across, with a double tectum; style arm hairs often rounded, only ± at the tip, stigmatic surface as two marginal bands; pump-type secondary pollen presentation common; (cypsela with phytomelanin), (pappus paleaceous); n = (4-)9-10(-19 - Heliantheae, etc.); rbcL 6bp x 4 inversion, (5S and 35S ribosomal genes associated).
1,135/17,200: Senecio (1250), 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), Pseudognaphalium (90), Symphyotrichum (90), Felicia (85), Fleischmannia (80), Pluchea (80), Pulicaria (80), Pteronia (80), Espeletia (72), 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., as did Panero and Crozier (2016: Table S1) - (47.8-)43.2(-38.7) m.y., although most estimates are somewhat younger (Funk et al. 2009c), e.g. Pelser and Watson (2009), around 39-26 m.y., while at around 46 to 36.5 m.y. C.-H. Huang et al. (2016: three estimates) gives a choice.
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, esp. 2015, for which, see also Panero 2016, Barreda et al. 2016). Depending on the identification of the grains, the first eight subfamilies above may all have diverged by the late Eocene about 34 m.y.a.; other suggestions are of an (early) Oligocene radiation of the subfamilies (K.-J. Kim et al. 2005; Funk et al. 2005; M. S. Barker et al. 2008; Torices 2010), or all of these subfamilies, apart from the Cretaceous Barnadesioideae, diverging rapidly, perhaps within 10 m.y., in the Palaeocene-early Eocene by around 50 m.y.a. (Barreda et al. 2015; C.-H. Huang et al. 2016: Famatinanthoideae also diverged earlier). See also Funk et al. (2014) for dates.
Diversification of Asteraceae probably began in southern South America - distributions of the six basal clades are centred in South America, movement to Africa being by way of islands on what are now the Rio Grande Rise and the Walvis Ridge, and 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), and a woody/shrubby habit is common in several of these South American clades (Panero et al. 2104). With the earlier pollen-based date from the Antarctic suggested by Barreda et al. (2015) movement around high southern latitudes is also plausible. Many clades then arose in the course of a subsequent radiation from Africa (Panero & Funk 2008; Funk 2009; Funk et al. 2009c; see also Kim & Jansen 1995); Panero and Crozier (2016) suggest that the last six subfamilies in the list above - Carduoideae to Asteroideae - diverged within about 6.5 m.y. in the Middle Eocene in Africa. Thus both South America and Africa are central to our understanding of the early spread and diversification of the family, although Samant and Mohabey (2014) thought that Asteraceae originated in Late Cretaceous India.
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 (see Calabria et al. 2009, etc.), or some other reason (see also Funk et al. 2009c; Panero & Crozier 2016). For possible apomorphic characters for the family and its major clades, see e.g. Hansen (1991), Jansen et al. (1991), Bremer (1994), Leins and Erbar (2000), Erbar and Leins (2000), Funk et al. (2009c), Roque and Funk (2013), Panero et al. (2014) and Telleria et al. (2015: emphasis on Barnadesioideae). Burleigh et al. (2006) suggest that by some measures Asteraceae do show a notable shift (increase) in morphological complexity. There was a palaeopolyploidy event involving most or all of the family, and Schranz et al. (2012) thought that although there was a lag time between this duplication event and subsequent diversification of the family, the two might be causally linked (see also Tank et al. 2015). More attention should be paid to the significance of pollination of Asteraceae by oligolectic bees (see below).
There are perhaps parallels with Poaceae, which coincidentally also have large-scale genome duplications and store carbohydrates as fructans. Diversification in Asteraceae is 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 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 twelve clades basal to Asteroideae have relatively few to very few species (see also Panero & Funk 2008; Panero et al. 2014; Panero & Crozier 2016), although Cichorioideae have ca 3,600 species and Carduoideae ca 2,800 species. The successive subfamilies in the tree above have 92, 1, 637, 35, 48, 85, 1, 2,864, 70, 2, 3,994, 7, 17,200 species (figures from Panero & Crozier 2016), not surprisingly, evolutionary rates within the family are highly heterogeneous (S. A. Smith et al. 2011). Places where diversification rates seem to have changed are rather different in Panero and Crozier (2016, q.v. for more details), perhaps because of where they assign particular fossils and also because of their more detailed sampling; they suggest shifts at the [Cichorioideae [Corymbioideae + Asteroideae]] node and a largely American clade in Asteroideae-Heliantheae alliance whose fruits have phytomelanin. C.-H. Huang et al. (2016) also discuss diversification in the family in the context of possible genome duplications. They suggest that there were increases in diversification rates in the [Carduoideae + The Rest], within Asteroideae and in Barnadesioideae (the last only moderate), with decreases in diversification rates in Famatinanthoideae and Gymnarrhenoideae (C.-H. Huang et al. 2016).
Looking at individual subfamilies, at 2,400+ species the speciose Cardueae 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. Much of the diversification in the Mediterranean-Central Asian Carduoideae-Centaureinae may be Plio-Pleistocene transition and younger (Hellwig 2004). Diversification of the high-altitude species of Saussurea (Carduoideae-Cynareae) 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 J.-Q. Liu et al. (2006) advance a similar explanation for the diversification of the 200+ species of the Ligularia–Cremanthodium–Parasenecio clade (Senecioideae), relationships within which are largely unresolved, and there have been other radiations of Asteraceae in this area (J. W. Zhang et al. 2011 and references).
Bell et al. (2012b) suggest that there has been rapid diversification of Tragopogon et al. (Cichorioideae) in Eurasia, probably ca 2.6 m.y.a. or at least within the last 5.4 m. years. Dispersal of Arctotidae-Arctotidinae from South Africa to Australia probably happened within the last 14 m.y., more probably (4.4-)3(-1.7) m.y. (McKenzie & Barker 2008).
For some divergence dates in Asteroideae, see C.-H. Huang et al. (2016: table S3). Asteroideae-Gnaphalieae include over 1,200 species. The crown-group age is (35.3-)29.4(-24) m.y., and the three basal clades are from southern Africa, the other main clades also originating there, overall, an African origin for the tribe (Nie et al. 2016). Australasia was the next area to been colonized, and most speciation in the tribe as a whole has been within the last 23 m.y., i.e. is Miocene or younger (Nie et al. 2016, q.v. for much more detail). Bergh and Linder (2009) date Gnaphalieae to (52.3-)34.5(-20.6) m.y.a., the stem age of the some 550 species of the Australasian part of the tribe being (22.1-)15.6(9.1) m.y., and the crown age (20.6-)14.6(-8.3) m. years. For some character evolution in Inuleae (inc. Plucheeae), see Nylinder and Anderberg (2015). Plucheinae are commonly plants of arid conditions that may have originated in southwest Africa (Namib, Kalahari) (Nylinder et al. 2016). 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 a polyphyletic Psiadia to Madagascar and thence to the Mascarenes.
The Hawaiian clade that includes the silversword, Argyroxiphium sandwicense, is descended from herbaceous tarweed-like ancestors of the Madia-Raillardopsis group (Helenieae-Madiinae) from western North America. With some 33 species (placed in three genera) that diversified (6-)5.2(-4.4) m.y.a., it is a classic example of hybridization followed by an adaptive radiation that includes trees, shrubs, cushion plants, and of course the remarkable silversword, a monocarpic rosette plant (see e.g. Baldwin & Sanderson 1998; Baldwin & Wessa 2000; Carlquist et al. 2004; Shaw & Gillespie 2016 for the progression rule, also the Madiinae Showcase). Variation in foliar functional traits like venation density approaches that in angiosperms as a whole, but it shows little correlation with phylogeny (Blonder et al. 2016). The closest relatives of another Hawaiian endemic, Hesperomannia, with three species, are African Vernonieae (Kim et al. 1998); divergence of Hesperomannia from Vernonia has been dated at around 26-17 m.y.a., old for a Hawaiian endemic (Kim et al. 1998), so there has presumably been intra-archipelago island hopping. Bidens is also very diverse on Hawaii with more variability in growth form, etc., than in the rest of the genus, but as with these other taxa, there is little in the way of molecular variation or genetic barriers between the species (Ganders et al. 2000; see also Keeley & Funk 2011).
The iconic stout-stemmed (pachycaul) giant senecios (some = Dendrosenecio) of the African mountains are mostly closely related, but are not immediately related to one another, representing a 4-14 independent movements into alpine habitats (Knox & Palmer 1995a, b; Pelser et al. 2007; Kandziora et al. 2016b). The clade involved probably became adapted to montane conditions in the Drakensberg, to the south (Kandziora et al. 2016b) and subsequently colonized the Palaeoarctic, probably twice, one clade including annuals (inc. S. vulgaris) the other perennials of the mountains (Kandziora et al. 2016a). Within Senecio s. str. there has been intercontinental dispersal between areas with Mediterranean and desert climates (Coleman 2003). Espeletia is a characteristic genus of the Andean páramo, and it, too, is secondarily woody and often more or less pachycaul, and other Asteraceae are to be found in this habitat (Sklenár et al. 2011 and references). Indeed, the around 144+ species of Espeletiinae, which diversified (5.9-)4(-2.4) m.y.a., represent a substantial and rapid diversification there (Madriñan et al. 2013; Lagomarsino et al. 2016), with more or less independent radiations in the Venezuelan (older) and Colombian páramos (Diazgranados & Barber 2017). As Small (1919: p. 142) noted of the ability of Asteraceae to colonize places like Krakatau, "The Compositae, indeed, seem to have been formed with the mountains by the mountains for the mountains.".
Evolution of the considerable variation in pollen morphology in Asteraceae has often been understood using the distorting lens of pollen "types". However, Blackmore et al. (2009; see also Skvarla et al. 1977 for pollen terms) decompose these types into a number of individually-varying characters - note that some are divisions of continua - and then discuss their distribution on the Asteraceae tree; pollen characters provide apomorphies at various levels. 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 caveae are evident early in development in Gerbera (Mutisieae), but not later, and suggested that pollen grains of Asteraceae might all be caveate - however, the very definition of caveate is unclear (Blackmore et al. 2009). Blackmore et al. (2010), in a very interesting review, discuss pollen development, showing how self assembly of many pollen features is common, but that changes in the glycocalyx, the primexine matrix and made up of glycoproteins, and in pH, etc., affect details of self assembly, and some of this more proximate variation is probably under genetic control.
Although Asteraceae are worldwide in distribution, around 14% of all Asteraceae - ca 3,300 species - are to be found in Mexico, Asteroideae-Eupatorieae alone having around 530 of its ca 2,000 species there (Schilling et al. 2015 and references).
Ecology & Physiology. Growth form is notably labile in Asteraceae compared with that in other campanulids, and many taxa are woody-herbaceous intermediates (Beaulieu et al. 2013b: the character there = woody vs herbaceous, but c.f. e.g. Carlquist 2013). Woody Asteraceae are common on ecological/actual islands, i.e. including mountains throughout the tropics, where the evolution of woodiness is common (e.g. Carlquist 1974). Climbing Asteraceae are prominent in montane forests of South America, some 470 scandent species being reported from the New World (Gentry 1991).
Plucheinae (Asteroideae-Inuleae) are prominent in arid floras of the Southern Hemisphere (Nylinder et al. 2016). 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; T. Sage et al. 2013; Christin & Osborne 2014; Lyu et al. 2015: RNA-seq data, some differences in topology); there are also proto-Kranz species (R. Sage et al. 2014). Christin et al. (2011b) suggest a number of dates for C4 origins 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 in the evolution of C4 photosynthesis in other groups.
For selenium hyperaccumulation, see references in Schiavon and Pilon-Smits (2016).
Pollination Biology & Seed Dispersal.
The capitulum can become reduced to a single flower, the single-flowered capitulae may then aggregate into a supercapitulum, and there may even be yet another round of aggregation (Claßssen-Bockhoff 1996b for details; Harris 1994 [Caenozoic capitulae], 1999; Leins & Gemmeke 1979; Katinas et al. 2008a). Supercapitulae have evolved at least three times in Lactucoideae-Vernonieae, perhaps with reversion to normal capitulae (Loeuille et al. 2015a), and a couple of times in Inuleae s.l. (Nylinder & Anderberg 2015). (Supercapitulae have sometimes been thought to be of taxonomic importance - Loeuille et al. 2015a.) Whether an ordinary 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). Disc flowers are quite often polysymmetric and the ray flowers monosymmetric. This monosymmetry seems to be caused by the CYC2c gene family, different members of which have been independently coopted by different taxa in Asteraceae (Chapman et al. 2010). Although the genes involved in the development of monosymmetric flowers of Senecio vulgaris are homologous to those in Antirrhinum (Plantaginaceae) they are regulated and expressed differently, growth in the adaxial part of the corolla being reduced and that in the abaxial part increased, hence the ray phenotype (Garcês et al. 2016). Of course, the common ancestor of Plantaginaceae and Asteraceae is likely to have had polysymmetric flowers (see Euasterids below). Interestingly, Dasyphyllum (Barnadesioideae) lacks members of the CYC2b, d and e gene families common elsewhere in Asteraceae, while Acicarpha (Calyceraceae) also lacks CYC2c genes (Chapman et al. 2010).
Secondary pollination mechanisms can broadly be divided into three types - the drag type, pollen grains attaching to microhairs on the style, the brush type, where hairs on the outside of the style/style arms sweep up the pollen, and the brush type, pollen being swept up by hairs on the apices of the style arms; these types tend to predominate in particular subfamilies (Anderberg et al. 2007; Erbar & Leins 2015: a slightly different typology). Leins and Erbar (2003b) suggest an evolutionary sequence for pollen presentation devices, and later they optimise features involved in such devices on a phylogenetic tree, the emphasis being on the basal pectinations of the family - as they note, variation is extensive there, perhaps especially so in Barnadesioideae (Erbar & Leins 2015). Within Barnadesioideae, sister to the rest of the family, secondary pollen presentation is by the drag type (as in at least some Calyceraceae) or by an unspecialised type of brush mechanism (e.g. Erbar & Leins 2000, 2015; 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 general, insect - especially bee - pollination occurs throughout the family, for bird and wind pollination, see below. 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, but similar associations occur in Europe. 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 (see also Fowler 2016). Thus some species of north temperate Colletes (plasterer bees) specialize on Asteroideae, other species rarely visiting them; specialization on flowers of Asteraceae has evolved three or four times there (Müller & Kuhlmann 2008). Several species of oligolectic bees may visit the one composite species (Linsley 1958; Moldenke 1979b; Lane 1996; Müller & Kuhlmann 2008; Praz et al. 2008; Kuhlmann & Eardley 2012; Vogel 2016). Pollination in Helianthus (sunflowers) has been particularly well studied. Again, 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 bees visiting 21 species of Helianthus regularly for pollen. At most few were of these were obligately associated with Helianthus, most also working other species of Asteraceae; all told, 284 species of bees visited sunflowers for pollen, 128 species for nectar (Hurd et al. 1980; also Minckley et al. 1994). (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.) In the western Palaearctic about one third of the megachilid anthidiine bees studied (26/72) specialized on Asteraceae - this was five times more than the next family, Fabaceae - and all but two of these specialized on a single tribe (Müller 1996).
However, the story is more complicated - and interesting. Pollen of Asteraceae-Asteroideae and -Cichorioideae, at least, may be unsuitable food for many bees. It may lack essential amino acids, have generally lower amino acid (e.g. arginine in Asteroideae) and protein concentrations than other pollen, or contain harmful secondary metabolites (Waser et al. 1996; Müller & Kuhlmann 2008; Praz et al. 2008; Goulson 2010; Sedivy et al. 2011). Consequently, some bees actively avoid collecting pollen from composites, and if bees that are not Asteraceae specialists are fed pollen of Asteraceae, their larvae may die (Sprear et al. 2016 for references). 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). This would not stop them being effective pollinators (and might even enhance their effectiveness - dirty bees pollinate better). Brood parasitism (kleptoparasitism) is common is the solitary bees that are common on Asteraceae, yet nests of the megachilid Osmia mason bee feeding on asteraceous pollen (but not those feeding on pollen from other families of plants) were never parasitized by Sapygia wasps, and survival of the larvae of these wasps was reduced when they were fed pollen of Asteraceae (Spear et al. 2016).
Barreda et al. (2010b, 2012a) suggested that the flowers of Raiguenrayun, known from the Middle Eocene of Patagonia ca 47.5 m.y.a., might be pollinated by birds, but hummingbirds, the iconic bird pollinators of the New World, are known only from Europe at that time (e.g. Mayr 2004), so bird pollination is unlikely/other birds were involved (see also Panero et al. 2014). Bird pollination is rather uncommon in Asteraceae (Cronk & Ojeda 2008; Erbar & Leins 2015), although Vogel (2016) suggested that at least 60 species of the family were pollinated by birds, and around 45 of these were pollinated by hummingbirds.
In the 500< species of wind-pollinated Asteroideae the heads usually 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).
Breeding systems in the family are very diverse (e.g. Burtt 1961, 1977a), and the evolution of different flower types in Inuleae (Asteroideae) has been examined by Torices and Anderberg (2009). Although protandry is very common, when there are different flower types, interfloral protogyny predominates (Bertin & Newman 1993). Dioecy has evolved from monoecy and back again in Leptinella (Cotula s.l.: Himmelreich et al. 2012). Apomixis is common in Asteraceae, especially in Cichoroideae (Taraxacum - see Taraxacum absurdum van Soest, Hieracium, Crepis) and Asteroideae (Gnaphalium, Antennaria) (Asker & Jerling 1992; Hojsgaard et al. 2014; Hörandl et al. 2007 and references); Babcock and Stebbins (1938) remains a classic account of an agamic complex (see also Sears & Whitton 2016).
Most fruits are crowned by a plumose pappus, a highly modified calyx, which may be uni- to pluriseriate, associated with other pilose structures, or there may be scales of varyious morphologies and positions (Yu et al. 1999; Glover et al. 2015: confirmation at the level of gene expression; Small 1918; Mukherjee & Harris 1995; Mukherjee & Nordenstam 2008 and references 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); for myxocarpy, see Western (2011), and for "seed" dimorphism, see Song and Wang (2015 and references), with different fruit types from the one capitulum having different germination requirements.
Plant-Animal Interactions. The flowers of some Senecioneae and Eupatorieae (Asteroideae) are visted by male Danainae and Ithomiinae (butterflies) and Arctiinae and Ctenuchidae (moths) and of larvae of Arctiinae because the pyrrolizidine alkaloids they contain form the basis of their pheromones, or of compounds that other organisms find distasteful (see also Crotalaria, Apocynaceae, Boraginaceae and and Heliotropaceae: Edgar et al. 1974; Fiske 1975; Ackery & Vane-Wright 1984; Brown 1987; Weller et al. 1999; Anke et al. 2004). Zaspel et al. (2014) discuss the phylogeny of Arctiinae and the evolution of pharmacophagy there, and caterpillars may east the plants (Hartmann 2009; other articles in Conner et al. 2009). These two tribes of Asteroideae are not immediately related, so there has been parallel evolution of these alkaloids within the subfamily (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) (Pasteels et al. 2001; Termonia et al. 2002; Hartmann et al. 2003). Sesquiterpene lactones from Asteraceae are also sequestered by insects (e.g. Pasteels et al. 2001).
Pyrrolizidine alkaloids protect the plants that have them against some herbivores, although 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). The phytomelanin of the black cypselas in plants of the Heliantheae alliance may protect the fruits from dessication and also from the attentions of insect larvae (Pandey et al. 2014). See Calabria et al. (2009) for literature on the effects of asteraceous metabolites on insects.
Caterpillars of Nymphalidae-Melitaeini butterflies are common on Asteraceae, as well as 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 this case without a change in diversification rates (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 (Asteroideae) 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. For cecidomyiid galling, see Stireman et al. (2010).
A number of Asteraceae are quite densely and viscidly hairy, and insects may be trapped by the leaves, and eaten by mirid bugs in particular that are able to walk easily in such conditions (Wheeler & Krimmel 2015; LoPresti et al. 2015). Nitrogen, mainly ultimately from the trapped insects, may be taken up by the leaf (Spomer 1999).
Bacterial/Fungal Associations. Ectomycorrhizae have been reported from a number of Australian Gnaphalieae (Warcup 1990), but there is no recent work on thee plants. 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 M. S. Barker et al. (2008), Schranz et al. (2012) and C.-H. Huang et al. (2016). There was an early palaeopolyploidy event involving most or all of the family, and again near the base of Asteroideae and within Mutisioideae. These have been placed somewhat more precisely; one duplication (= a palaeotetraploidy) is at the [Calyceraceae + Asteraceae] node, but the position of the other, which resulted in a palaeohexaploidy, is still uncertain - above Barnadesioideae and below Carduoideae (see Barker et al. 2016a; C.-H. Huang et al. 2016). The pattern of duplicate gene retention is distinctive - structural/cell organization genes, but fewer regulatory genes were retained (Barker et al. 2008). A genome duplication in Lactuca, perhaps the first such event mentioned above, has been dated to (60-)58.3(-55.6) m.y.a. (Vanneste et al. 2014a).
Panero and Crozier (2016) discuss genome duplications and subsequent reductions in chromosome numbers in the family in some detail, with diploidization on occasion perhaps being linked with diversification. C.-H. Huang et al. (2016: Fig. 5) provide haploid numbers for some subfamilies and tribes, and these would suggest that x = 27 could be the basal number for the family as a whole.
For satellite DNA diversification in Cardueae, see del Bosque et al. (2014). The 5S and 35S ribosomal genes have become associated in Asteroideae, but they are separate in the other subfamilies, as is the usual condition for flowering plants (Garcia et al. 2010b).
A large inversion in the chloroplast genome occurs in most of the family, but not in Barnadesioideae and other Asterales (Jansen & Palmer 1987; Bremer 1987; see also below).
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 (and classification) 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; Galbany-Casals et al. 2014). 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; see also Galbany-Casals et al. 2014) 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 1,240 species of the tribe. For some hybridization between members of different subtribes in Cichorioideae, see Y. Liu et al. (2013) and between genera in Lactucoideae-Vernonieae-Lychnophorinae, see Loeuille et al. (2015b).
For recent hybridization/speciation in Senecio and Tragopogon and its significance, see Soltis et al. (2016b and references). Vallès et al (2012) discuss polyploidy and its connection with genome size, etc., and Vallès et al. (2013) summarize genome size variation in the family, although unfortunately little is known about genome size in the basal pectinations. For the reduction of chromosome numbers in Gnaphalieae, e.g. from n = 12 to n = 3 in Podolepis, see Smissen et al. (2011 and references).
Economic Importance. Timme et al. (2007) provide a phylogeny of 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.
Asteraceae produce tens of thousands of secondary metabolites (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.
Vegetative variation in the Kleinia-"Senecio" area is considerable, some species having very succulent terete or even almost spherical leaf bldes, or the stems may be succulent and the leaves early deciduous. Leaves of species like S. meuselii may be terete or laterally flattened and so appear to be equitant (see also Timonin et al. 2015).
For capitulum development, see above. Note that the floral bracts in some Asteroideae-Heliantheae (the tribe includes taxa that were in Eupatorieae) 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). In general, the very different adult floral morphologies found in Asteraceae are quite similar early in development (Harris 1995). 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. For theories as to the origin of the pappaus as other than a simple modified calyx, see Harris (1995) and Bello et al. (2013). 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, rather than in the adaxial petals, as in other core eudicots (Citerne et al. 2010).
Floret morphology varies extensively in Asteraceae, and this variation needs to be put in the context of the tree, which I have barely begun to do. 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 (0:5), but they may be a modified 2:3 bilabiate corolla in which the adaxial lobes have been suppressed (Weberling 1989; Gillies et al. 2002); true slit-monosymmetric flowers are uncommon here. Some taxa, including Barnadesioideae, have a midvein in the petal (see also Carlquist 1976; Gustafsson 1995); corolla variation in Barnesdeioideae alone is extensive (Stuessy & Urtubey 2006). The bicellular 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.
Details of the apex and base of the anthers have been much used in classification. Thus Senecio s. str. has balusterform filament collars (Salomón et al. 2016) - one can think of the filaments as being abruptly swollen near the apex. Wortley et al. (2007b, 2012) used distinctive pollen characters to help place some genera whose relationships had previously been unclear. See also Roque and Silvestre-Capelato (2001: pollen of Gochnatioideae), Wortley et al. (2008: Arctotidae-Cichoridoideae), Zhao et al. (2006: Mutisieae), Wortley et al. (2009, 2012: comprehensive bibliographies of palynological work), Tellería and Katinas (2009: Mutisia), Osman (2009: Cichorioideae-Cardueae), Hong Wang et al. (2009b: Cichorioideae-Cichorieae). There is considerable variation in tapetum "types" in the family (Pacini 1996).
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. Styles and style arms show much variation in indumentum/cell surface type, the distribution or receptive tissue, style arm length and apex and there is also variation in pollen presentation type. This is incompletely integrated with with the subfamilies above: see Erbar and Leins (2015: hair morphology, 2015b: styles and secondary pollen presentation) and Erbar (2015: multiseriate [= laterally connate] hairs on style, 2016: style morphology of basal asteraceous clades).
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. The cells of the integument have been described as commonly being some kind of "nutritive tissue" (Kolczyk et al. 2014). 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 other information on Asteraceae, see e.g. Carlquist (1976: variation in the context of a tribal classification), K. Bremer (1987, esp. 1994: classification rather different from that above, 1996: subfamilies), Hind et al. (1996), Katinas et al. (2008b: Mutisioideae), and Freire et al. (2014: esp. Famatinanthus). See also Katz et al. (2014: phytoliths and their possible function, no effect on larger herbivores), Thomas et al. (2009: development of Gorteria flowers), Vogel (1998c), Wist and Davis (2006) and Erbar (2014), nectaries and nectar secretion, Goldfluss (1898-9: antipodal cells), Small (1919: esp variation in embryo sacs), Grau (1980: testa structure, considerable amount of variation), and Watanabe et al. (2007), Dahlgren (1924: endosperm development), Semple and Watanabe (2009) and Watanable (2015), chromosome numbers.
Phylogeny. There has been much phylogenetic work on Asteraceae, and only a few of the older references are included. Panero and Funk (2002, especially 2008; see also Funk et al. 2005, a supertree, 2009c, a metatree) and Panero et al. (2014) present a phylogeny many details of which are reflected in the classification above. 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 (see Jansen & Palmer 1987; Bremer 1987; see also Y.-D. Kim & Jansen 1995; Jansen & Kim 1996; 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). Morphological data suggested to Roque and Funk (2013: c.f. character states) that Wunderlichioideae and Stifftioideae might form a clade, and there is also some molecular support for this clade (Funk et al. 2014). In the latter study, there was still weaker support for a [Mutisioideae + Stifftiodeae] clade and Perytoideae were outside a [Cichorioidae + Carduoideae] clade, but the latter areas were not the focus of the study and so sampling was poor (Funk et al. 2014). Fu et al. (2016: focus on Chinese taxa) found that Stifftioideae, Wunderlichioideae and Gochnatioideae all formed a clade. Gymnarrhena was excluded from Asteroideae by Anderberg et al. (2005) and it has maintained its current position since.
Fu et al. (2016) provided a comprehensive phylogeny of 200 genera of Chinese Asteraceae, and the supermatrix they examined included 512 genera all told, somewhat less than one third the total; see also Z.-D. Chen et al. (2016) for Chinese Asteraceae.
With the realization that the recently-rediscovered Famatinanthus was rather different from other Mutisioideae-Onoserideae, Panero et al. (2014: 14 loci, all chloroplast) examined basal relationships in Asteraceae. Famatinanthus was strongly supported as sister to the rest of the family bar Barnadesioideae, and Mutisioideae was the next branch, also with strong support, although support for the monophyly of Mutisioideae themselves could be better. Support for the positions of the next three clades up was also quite good (Panero et al. 2014; see also Panero & Crozier 2016). Taking a rather different tack, Mandel et al. (2014, 2015) looked at a massive conserved orthologous set of nuclear genes, and found that Centrapalus pauciflorus had sprung outside the other Cichorioideae examined, however, sampling was poor.
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; [Huarpea + Barnadesia] may be sister to the rest of the subfamily. For corolla morphology here, see Stuessy and Urtubey (2006).
Funk et al. (2016) recently added two genera in a separate subtribe to Mutisioideae, while Pasini et al. (2016) examined relationships around Gerbarea.
Funk et al. (2014, as tribes) discuss relationships in Gochnatoideae and Wunderlichioideae; genera like Cyclolepis remain hard to place.
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).
For the limits of Gymnarrhenoideae, see Anderberg and Ohlson (2012).
Cichorioideae: Warionia may be sister to all other Cichorieae (Kilian et al. 2009); although no flavonoids have been reported from this tribe, they are diverse in the rest of the subfamily (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; for relationships within Scorzonerinae, see Mavroidiev et al. (2004). 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 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 Bell et al. (2012b), and of the African Arctotideae-Gorteriinae, see Funk and Chan (2008) and the -Arctotidinae, see McKenzie and Barker (2008); in the latter, at least, genera are not monophyletic. For a phylogeny of Vernonia (Vernonieae), a genus whose circumscription is problematic - either it is huge, or quite small - see Keeley et al. (2007); Loeuille et al. (2015a) found four main clades within the American Vernonieae, although relationships between them were unclear, and within Lychnophorinae, one of these clades, relationships may be [Albertinia [[Blanchetia + Gorceixia] + The Rest]] (these three genera are monotypic), and within The Rest, mostly plants of the Cerrado, much of the spine was poorly resolved (Loeuille et al. 2015b). For relationships in the largely Peruvian Liabeae, sister to Vernonieae, see Funk et al. (2012).
Asteroideae: Relationships within this very large clade are still poorly understood (Bentley et al. 2015). 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 there is extreme polyploidy in Leptinella in particular (Himmelreich et al. 2014). 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.). 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. Within Gnaphalieae, morphological variation was analyzed by Anderberg (1991a), and phylogenetic relationships there have begun to be disentangled by Bayer et al. (2000), Nie et al. (2016) and others. Nie et al. (2016) found the relationships [Relhania clade [Metalasia clade [Lasiopogon + The Rest]]]. Helichrysum is polyphyletic (Galbany-Casals et al. 2004, 2009, 2010, 2014; Bergh & Linder 2009); Ward et al. (2009), Montes-Moreno et al. (2010), Nie et al. (2013: Anaphalis embedded in Helichrysum), Bengtson et al. (2015 and references: the South African Metalasia, also diversification), Schmidt-Lebuhn et al. (2015) and Weber and Schmidt-Lebuhn (2015), some odd Australian taxa, and Bentley et al. (2015: odd African Philyrophyllum, actually in Athroismeae) further clarify relationships in this tribe; there has been hybridisation (see above). For Mexican Eupatorieae, especially Brickeliia, see Schilling et al. 2015). For the phylogeny of the helenioid Heliantheae, see Baldwin et al. (2002). For the phylogeny of Inuleae (inc. Plucheeae), see Anderberg et al. (2005), Englund et al. (2009) and especially Nylinder and Anderberg (2015); morphological relationships in Inuleae and Plucheeae were discussed by Anderberg (1991b, c). Nylinder et al. (2016) discuss the phylogeny of Plucheinae. The sections of Blumea (Inuleae) need overhaul, see Pornpongrungrueng et al. (2009). Millerieae include Espeletia and relatives, frailejones, relationships within which are discussed by Diazgranados and Barber (2017: a fair amount of hybridization). 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); J.-Q. Liu et al. (2006) discuss relationships in the large Ligularia–Cremanthodium–Parasenecio clade, a major part of the Senecioneae-Tussilagininae. For relationships within Euryops, see Devos et al. (2010). For Symphyotrichum and relatives, see Vaezi and Brouillet (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, see the accounts there). Applying the same principles for subfamilial recognition (numbers of subfamilies) here as used effectively in Orchidaceae would, however, result in an heterogeneous Asteroideae of around 22,500 species (c.f. Chase et al. 2015).
Anderberg et al. (2006) enumerated the genera in the family, however, generic limits in many places are in a state of flux (see Kadereit et al. 2016 for European genera). 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)? Indeed, Senecio species are found scattered in eight clades or so, 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), -Astereae (e.g. Li et al. 2012), -Millerieae (Espeletia and relatives: Diazgranados & Barber 2017), Lactucoideae-Arctotidinae (McKenzie & Barker 2008), etc.. Genera in the Gochnatia area have been split, despite protestations: "we simply seek to insure [sic] that our classifications reflect what we know about evolution" (Funk et al. 2014: p. 879) - one wishes life were so simple. Finally, hybridisation (see above) makes some genera and even subtribes non-monophyletic. A suggested nomenclatural solution for the area around Helichrysum sounds like a slowly-unfolding disaster, but the alternative, a Helichrysum s.l., seems little better (Galbany-Casals et al. 2014).
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.