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].


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].


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].


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.


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; 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 [5], G [3] 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).



[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 [2], 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.



[GARRYALES [GENTIANALES, VAHLIALES, SOLANALES, BORAGINALES, LAMIALES]]: G [2], superposed; loss of introns 18-23 in RPB2 gene d copy [?level].

[GENTIANALES, VAHLIALES, SOLANALES, BORAGINALES, LAMIALES]: (herbaceous habit widespread); (8-ring deoxyflavonols +); vessel elements with simple perforation plates; nodes 1:1; C forming a distinct tube, initiation late [sampling!]; A epipetalous; (vascularized) nectary at base of G; style long; several ovules/carpel; fruit a septicidal capsule, K persistent.   Back to Main Tree

Age. Magallón and Castillo (2009) offer estimates of ca 81 m.y. for both relaxed and constrained penalized likelihood datings for this clade - but Vahliaceae are excluded. The age for the same node in Bell et al. (2010) is (96-)87, 83(-77) m.y. (again, Vahlia excluded) or (102-)92, 86(-79) m.y. (Vahlia included), in Bremer et al. (2004) it is ca 108 m.y., in Foster et al. (2016a: no Vahliales) it is ca 96 m.y., in Xue et al. (2012) it is only 60.4 or 57.6 m.y. and Naumann et al. (2013) 80.8(Boraginales excluded)-76.5 m.y., while in Nazaire et al. (2014) it is (102.1-)89.1(-73.3) m.y. - but c.f. topologies. The age of this node is estimated to be around 113 m.y. by Z. Wu et al. (2014: Boraginales sister to the rest) and ca 76.3 m.y. by Tank et al. (2015: Table S1).

Evolution: Divergence & Distribution. Magallón and Sanderson (2001) and Magallón and Castillo (2009) found high diversification rates in the four large orders, and the herbaceous habit (see S. A. Smith & Donoghue 2008) is also common here.

There are several characters of potential phylogenetic interest in this group. The hydroxycinnamic acid depside, rosmarinic acid, is known from Boraginaceae and Hydrophyllaceae, as well as some Lamiaceae (Mølgaard & Ravn 1988). Lamiales and Boraginaceae have in common similar hydroxycinnamic acid derivatives, i.e. disaccharide esters of rosmarinic/lithospermic/caffeic acids (Mølgaard & Ravn 1988). Oleaceae, Lamiaceae, and Solanaceae have (arabino)xyloglucans and some (galacto)xyloglucan hemicelluloses in the cell wall; the plesiomorphic condition for seed plants is to have (fuco(galacto))xyloglucans (O'Neill & York 2003; Harris 2005), but the sampling is very poor. Boraginaceae have callose plugs in the pollen tube, as do Solanales, but their presence varies in Hydrophyllaceae, and they are absent in Heliotropiaceae, Cordiaceae, and monosymmetric-flowered Lamiales (Cocucci 1983). Protein crystals in nuclei are common, but are apparently not known from Avicennia, etc. (Speta 1977, 1979), and information is needed for groups recently moved to Lamiales. Whether or not such crystals characterise both Lamiales and also Boraginaceae s. str. (see also Wagstaff & Olmstead 1997) needs to be confirmed. Although some Boraginaceae have protein bodies in their nuclei, they are of two very different kinds, and many Boraginaceae entirely lack them; there is also variation within Lamiales.

González and Rudall (2010) thought that a bicarpellate gynoecium might be an apomorphy for this clade, and it was perhaps derived from a pseudomonomerous gynoecium like that of Metteniusa (Metteniusaceae) - see also for gynoecial evolution.

Pollination Biology & Seed Dispersal. These lamiids include many large- and monosymmetric-flowered taxa that have dry fruits with many seeds, although Convolvulaceae, Lamiaceae, and Verbenaceae, for example, have a maximum of four seeds/fruit. However, even when each fruit has fewer seeds, these are generally small. Euasterids as a whole commonly have rather small seeds (Linkies et al. 2010), perhaps to be expected, being connected with the herbaceous-shrubby habit so common there, and this contrasts with the larger seeds of most Aquifoliales, Icacinales, etc., that are basal in the lamiids and campanulids (see also Moles et al. 2005a).

Plant-Animal Interactions. Nylin et al. (2014) noted that members of all four orders were hosts for nymphalid butterfly larvae, three (but not Boraginales) being "important" hosts - only seven orders in this category were mentioned.

Chemistry, Morphology, etc. Hoffman et al. (2005) found that the xyloglucans of the few Solanales and Lamiales they examined lacked fucosylated subunits; the one Gentianales they examined was intermediate. This clade (bar Boraginales) may have closed root apical meristems (Clowes 2000), but the sampling is poor.

Phylogeny. Relationships in this part of the tree have long been unclear. Thus Bell et al. (2010) suggested the grouping [Lamiales [Gentianales [Boraginaceae [= Boraginales hereafter] + Solanales]]], Lens et al. (2008a: Bayesian analyses) and Magallón and Castillo (2009) that of [Gentianales [Lamiales [Boraginales + Solanales]]], and Lens et al. (2008a: maximum parsimony) found the relationships [[Solanales + Gentianales] [Lamiales + Boraginales]]. Qiu et al. (2010: mitochondrial genes) did not find Boraginales and Gentianales to be immediately associated, although they were not strongly separated, while the two were sometimes linked, if with weak support, by Ruhfel et al. (2014: see also other positions for Boraginales). In general, relationships between Gentianales, Lamiales and Solanales remained uncertain (Albach et al. 2001b; B. Bremer et al. 2002; Janssens et al. 2009, Boraginales not included; J. Li & Zhang 2010). Even an analysis of all 79 protein-coding plastid genes and four mitochondrial genes did not clarify them (Moore et al. 2008) nor did the 17-gene 640-taxon study of Soltis et al. (2011). Finet et al. (2010) found quite good support for a [Gentianales + Solanales] clade, but no Boraginales were included.

Weigend et al. (2013b), sampling four plastid loci and 134 taxa (81 Boraginales), found the very weakly supported sets of relationships [Boraginales [Lamiales [Solanales + Gentianales]]] (see also Nazaire et al. 2014: Suppl. Fig. 4A, ITS + 4 plastid markers) and [Lamiales [Gentianales [Solanales + Boraginales]]] in different analyses. The [Solanales + Boraginales] clade was recovered by Luebert et al. (2016b), but the position of Gentianales was unclear. Cassinopsis (Icacinaceae) was strongly supported as sister to the whole lot. In chloropast genome analyses, the relationships [Lamiales [Boraginales [Gentianales + Solanales]]] were recovered by Ku et al. (2013; for [Gentianales + Solanales], see also Martínez-Alberola et al. 2013), while Boraginales were sister to the rest in the study by Z. Wu et al. (2014: relationships not strongly supported). On the other hand, Refulio-Rodriguez and Olmstead (2014), sampling 1 mitochondrial and 9 plastid genes and 129 terminals (75 in Lamiales), recovered the relationships [Gentianales [Solanales [Boraginales + Lamiales]]]; the whole clade had very strong support, as did the monophyly of the orders, but bootstrap support for the two nodes along the spine was only moderate (maximum likelihood) or very weak indeed (maximum parsimony). The amount of data analyzed seems to have allowed somewhat improved support for these relationships, and their topology is used here to explore its morphological, etc., consequences (see also Tank & Olmstead 2017). However, the topology [[Solanales + Gentianales] [Boraginales + Lamiales]] was recovered by Magallón et al. (2015) and Z.-D. Chen et al. (2016: support very weak), while Maia et al. (2014), in one alignment using 18S/26S nuclear ribosomal data, retrieved a polyphyletic Boraginales within Solanales, although support was not strong, while another alignment suggested a clade [Boraginales + Gentianales]. The relationships [[Boraginales + Gentianales] [Lamiales + Solanales]] were recovered by Stull et al. (2015), but again support was not strong. One factor driving these conflicting relationships may be differing signals in nuclear (= [Solanales + Gentianales] clade) and chloroplast (= [Lamiales + Gentianales]] clade) genes (Xi et al. 2014), although Stull et al. (2015) looked at chloroplasts. The three compartments also yielded different topologies from each other (and differing from those in Xi et al. 2014) in Sun et al. (2014).

Furthermore, the position of Vahlia remains uncertain. Magallón and Castillo (2009), Magallón et al. (2015) and Bell et al. (2010) suggested that it was sister to all other lamiids (except Garryales, Icacinales, etc.). In both analyses of combined 18S/26S nuclear ribosomal data, Maia et al. (2014) found remarkably strong - given the weak support for most relationships in their study - support for this position. The genus was placed as sister to Lamiales, but with only 63% bootstrap support, by Albach et al. (2001b; see also Lens et al. 2008a: Bayesian analyses; Nazaire & Hufford 2012: plastid genes; Weigend et al. 2013b; Nazaire et al. 2014: Suppl. Fig. 4A), or it links with Boraginaceae in other analyses (Lundberg 2001e; B. Bremer et al. 2002). Only in ndhF analyses was there some support for a linkage with Solanales (Olmstead et al. 1999, 2000; see also Savolainen et al. 2000a; Lundberg 2001e). Refulio-Rodriguez and Olmstead (2014) also found this position, but despite the large amounts of data in their study, there was substantial support only in the Bayesian analyses. Stull et al. (2015) found Vahlia to be weakly linked with a [Solanales + Lamiales] clade, and in Tank and Olmstead (2017) the linkage was with a [Solanales [Boraginales + Lamiales]] clade. Vahlia was consistently found to be sister to Lamiales by Luebert et al. (2016b). The genus is now placed in the monogeneric Vahliales (see A.P.G. IV 2016).

GENTIANALES Berchtold & J. Presl  Main Tree.

Route I iridoids [mostly derived from secologanin or secologanic acid], monoterpene indole alkaloids, (O-methylated) flavones and flavonols +, non-hydrolysable tannins [e.g. myricetin] usu. 0; glandular hairs 0; pits vestured; nodes?; petiole bundle(s) arcuate; colleters +; branching from current flush; leaves opposite, joined by a line across the stem, (stipules +); (corolla swollen at the apex in bud); pollen orbicules +; ovules many/carpel, endothelium 0; endosperm nuclear, copious [?level]. - 5 families, 1,118 genera, 19,840 species.

Age. Crown-group Gentianales may be some (75-)71, 68(-65) or (68-)64, 61(-57) m.y. old (Wikström et al. 2001: the first age is with Dialypetalanthus sister to the rest, the second ignores D.). Janssens et al. (2009) date them to 79±10.2 m.y.; comparable figures are 108 and 78 m.y. in Bremer et al. (2004) while the ages in Wikström et al. (2015), at (104-)96(-87) m. y., and Olmstead and Tank (2017), at (105.6-)91.2(-75.2) m.y., are similar. Estimates of crown group ages are (86-)73(-60) (ages in Rubiaceae table) or (75-)52(-35) m.y. (ages in asterid table) in Lemaire et al. (2011b), (78-)69, 65(-54) m.y. (Bell et al. 2010) and ca 67.7 m.y.a. (Magallón et al. 2015); B. Bremer and Eriksson (2009) suggest rather greater ages of (104.7-)90.4(-76.5) m.y., as do Neupane et al. (2017: ((102-)89(-78) m.y.), while at around 58.8 m.y. ages in Tank et al. (2015: Table S2) are on the young side.

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).

Evolution: Divergence & Distribution. Wikström et al. (2015) discuss dates suggested for the order and for Rubiaceae by earlier workers, and mention a root age for Gentianales of 98-58 m.y.a. in B. Bremer and Eriksson (2009), but the latter give no root age.

Endress (2011a) suggested that a key innovation in Gentianales was tenuinucellate ovules.

Bacterial/Fungal Associations. Paris-type endomycorrhizae involving Glomeromycota are common in Gentianales, although some taxa may have the Arum type or intermediates, perhaps especially in Apocynaceae (Imhoff 1999).

Genes & Genomes. Coffea has no obvious genome duplication more recent than the core eudicot γ whole nuclear genome duplication, the gamma triplication (Denoeud et al. 2014).

Chemistry, Morphology, etc. For iridoid synthesis, see Jensen et al. (2002) and references. Wink (2008) noted that the enzyme strictosidine synthase, a key intermediary in the formation of the monoterpene indole alkaloids commonly found in Gentianales, is in fact quite widely distributed in flowering plants. The monoterpene indole alkaloid camptothecin is scattered through Gentianales, e.g. it is found in Opiorrhiza (Rubiaceae), Mostuea (Gelsemiaceae) and Ervatamia (Apocynaceae) (see Lorence & Nessler 2004).

Colleters range from secretory palisade cells surrounding an elongated axis to much smaller, simpler, hair-like structures (some Gentianaceae, Apocynaceae-Asclepiadoideae). They are borne on leaves, the calyx or corolla (Renobales et al. 2001), or even in a ring below the leaves and encircling the stem, as well as in their normal axillary position, and they may sometimes be vascularized, as in some Rubiaceae and Apocynaceae (Fernandes et al. 2016 and references). For variation in the composition of colleter secretion, see Resmondi et al. (2015). There are relatively few reports of colleters in Gentianaceae (Thomas 1991).

Tapetal variation is considerable, amoeboid tapeta being known from some species of Gentianaceae, Rubiaceae and Apocynaceae (Furness 2008a). Most families have taxa with bi- or tricellular pollen grains; for further discussion, see Williams et al. (2014). There is substantial variation in the presence of the mitochondrial coxII.i3 intron in this clade.

Some information is taken from Rogers (1986: general), Erbar and Leins (1996: corolla development), Conn et al. (1997: general), Jansen and Smets (1998: wood anatomy, 2000: vestured pits), and Vinckier and Smets (2002a, c: orbicules).

Phylogeny. Struwe et al. (1995) suggested that Loganiaceae, even when narrowly circumscribed, i.e. excluding Buddleja, etc., were extremely paraphyletic, with clades including about 1,300 genera and 15,500 species (Rubiaceae, Gentianaceae, Apocynaceae + Asclepiadaceae) coming from within them; they delimited families accordingly. However, B. Bremer (1996a), Potgieter et al. (2000) and Backlund et al. (2000) and authors since found rather different relationships - Rubiaceae are sister to Loganiaceae, Gentianaceae, Gelsemiaceae and Apocynaceae.

Relationships between these last four families remain unclear. M. Endress et al. (1996) found the relationships [Gelsemiaceae [Apocynaceae [Strychnaceae + Geniostomaceae (well supported)]], see also B. Bremer and Struwe (1992). In other analyses there is weak support for a relationship between Gelsemiaceae and Apocynaceae (Backlund et al. 2000; Jiao & Li 2007; see also B. Bremer 1999; Rova et al. 2002). However, B. Bremer et al. (2002) and Soltis et al. (2011: sampling) found some support for a sister group pair [Gentianaceae + Apocynaceae], as did Magallón et al. (2015) and Refulio-Rodriguez and Olmstead (2014: not the maximum likelihood analysis). Refulio-Rodriguez and Olmstead (2014) also found support for the pair [Gelsemiaceae + Loganiaceae], and their topology is provisionally folowed here (see also Struwe et al. 2014: weak support; Wikström et al. 2015). However, Tank and Olmstead (2017) recovered the relationships [Apocynaceae [Gentianaceae [Loganiaceae + Gelsemiaceae]]], L.-L. Yang et al. (2016) [Gentianaceae [Gelsemiaceae [Loganiaceae + Apocynaceae]]], but with little support, and Z.-D. Chen et al. (2016) the relationships [Gelsemiaceae [Loganiaceae [Gentianaceae + Apocynaceae]]], and with moderate support.

Previous Relationships. The circumscription and relationships of Loganiaceae are a key to understanding the both the past and present circumscription and relationships of Gentianales. Classically, Loganiaceae have seemed to show relationships with many sympetalous groups, and Bentham (1856) compared a broadly delimited Loganiaceae to a less-wooded area from which obvious forests representing more distinctive families such as Rubiaceae, Solanaceae, etc., had been removed. Loganiaceae in this sense (e.g. Leeuwenberg 1980) had ca 22 genera and 310 species. Of these genera, Buddleja s.l. and Androya (not immediately related), Peltanthera and Sanango (not immediately related), Plocospermum, Nuxia and Retzia, and Polypremum, are now in five or more separate clades in Lamiales (in Scrophulariaceae, Peltantheraceae, which are near Gesneriaceae, Gesneriaceae, Plocospermataceae, Stilbaceae and Tetrachondraceae respectively), while Desfontainia (Desfontainiaceae) is in Bruniales, a campanulid (for references, see those families), so it is not surprising that Loganiaceae seemed to be such a "central" family. Chemical variation within Loganiaceae s.l. strongly supports its break-up (e.g. Jensen 1999). However, Loganiaceae are morphologically quite heterogeneous even in their much more restricted circumscription.

Includes Apocynaceae, Gelsemiaceae, Gentianaceae, Loganiaceae, Rubiaceae.

Synonymy: Apocynales Berchtold & J. Presl, Asclepiadales Berchtold & J. Presl, Chironiales Grisebach, Cinchonales Lindley, Galiales Bromhead, Loganiales Lindley, Lygodisodeales Martius, Rubiales Berchtold & J. Presl, Strychnales Link, Theligonales Nakai, Vincales Horaninow

RUBIACEAE Jussieu, nom. cons.   Back to Gentianales


Plant woody; tanniniferous, triterpenes; (cork cambium deep-seated); true tracheids +; nodes 1(-3 or more):1(-3 or more), (+ split laterals); crystal sand +/0; secretory sacs widespread; stomata paracytic; lamina vernation usu. flat, stipules interpetiolar (sheathing; intrapetiolar; two pairs; toothed or not), innervated from circumferential vascular ring; inflorescences often thyrsoid, flowers often aggregated; flowers 4- or 5-merous, (heterostyly +); K small, aestivation open, (free), (0), C with early tube formation, C often left-contorted (valvate); ovary inferior, nectary on top, (placentation to parietal), style usually well developed, stigma wet or dry; ovules (apotropous), (parietal cells +), (nucellar epidermal cells anticlinally elongated), (endothelium +), (obturator +); megaspore mother cells several, (embryo sacs several, ± haustorial); fruit baccate, drupaceous, or septicidal, loculicidal or laterally dehiscent capsules, etc., (G largely superior in fruit); seeds 1-many, (pachychalazal; ruminate), exotesta alone persisting, papillate/short hairy or not, cells variously thickened, (mesotestal cells thickened); endosperm cellular or nuclear, often hemicellulosic, embryo straight to curved, (medium), suspensor haustorium + [?all]; n = 11 (10-16).

611[list]/13150 - in four groups below. World-wide, but largely tropical, especially Madagascar and the Andes (map: from Hultén 1958, 1971; Brummitt 2007). [Photo - Flower.]

Age. Antonelli et al. (2009) suggest that divergence within Rubiaceae began (68.8-)66.1(-63) m.y.a. similar to the ages in Olmstead and Tank (2017) of (83.8-)66.1(-50) m.y.a., although B. Bremer and Eriksson (2009) provided rather older dates of (100.8-)86.6(-72.9) m.y., and, at (98-)85(-74) m.y., also Neupane et al. (2017). Crown group ages in Lemaire et al. (2011b) are around (77-)62(-50) m.y., and (60-)56, 55(-51) m.y. in Wikström et al. (2001), (69-)57(-45) m.y. in Bell et al. (2010: note topology), (87.9-)84.9(-80.8) m.y. in Manns et al. (2012) and (96-)87(-79) m.y. in Wikström et al. (2015).

Graham (2009) summarized the fossil history of Rubiaceae - there are no certain records from the Cretaceous or Palaeocene, the earliest being vegetative fossils from the Eocene of North America (Roth & Dilcher 1979) which had previously been placed in seven families and four orders. These fossils are a little odd in that Roth and Dilcher (1979), who compared them with members of Cinchonoideae and Ixoroideae, suggested that the stipules on the petiole bases might be single, and at least sometimes they are minutely serrulate, perhaps because of hydathodes on their margins. Martínez-Millán (2010) dated the family to around 40.4. m.y. ago.

1. Rubioideae Verdcourt

Commonly herbs; (camptothecin + [pentacyclic quinoline alkaloid]), (cylcotide proteins +), (monofluoracetates +), anthraquinones from shikimic acid [rare elsewhere], iridoids, indole alkaloids common, plants Al-accumulators [esp. woody taxa]; (root with superficial cork cambium - Paederia); (wood rayless); raphides + [square in transverse section]; hairs septate, articulated; heterostyly esp. common; C often valvate, (tube with windows); (A not adnate to C); pollen grains (to 20-zonocolporate), (3-celled); ovules (few), (campylotropous), (apotropous), (apex of nucellus exposed), integument 1-14 cells across; (megaspore mother cells 2-15), (embryo sac tetrasporic, 15-16-celled, antipodal cells numerous [Crucianella - type]), (antipodal cells persist); (testa ca 14 cells across - Schradera; (suspensor haustorium +); loss of atpB promoter.

/7600: Psychotria s. l. (1600), Palicourea (600), Galium (400), Spermacoce (275: inc. Borreria), Oldenlandia (250), Notopleura (210), Hedyotis (200), Rudgea (200), Lasianthus (185), Chassalia (140), Coprosma (105), Argostemma (100), Gynochthodes (95), Margaritopsis (80), Gaertnera (70), Schradera (55), Morinda (40). Worldwide. [Photo - Fruit.]

Age. B. Bremer and Eriksson (2009) suggested ages of (90.7-)77.9(-65.3) m.y., Wikström et al. (2015: topology) ages of (85-)76(-67) m.y., and Lemaire et al. (2011b) ages of (60-)53(-48) m.y. for crown-group Rubioideae.

Synonymy: Aparinaceae Hoffmannsegg & Link, Asperulaceae Spenner, Cynocrambaceae Endlicher, nom. illeg. Galiaceae Lindley, Hedyotidaceae Dumortier, Houstoniaceae Rafinesque, Hydrophylacaceae Martynov, Lippayaceae Meisner, Lygodisodeaceae Bartling, Nonateliaceae Martynov, Operculariaceae Perleb, Pagamaeaceae Martynov, Psychotriaceae F. Rudolphi, Spermacoceaceae Berchtold & J. Presl, Theligonaceae Dumortier, nom. cons.

Luculia, etc., Cinchonoideae, Ixoroideae: plants woody; route II carboxylated iridoids +, indole alkaloids +; hairs mostly cylindrical; secondary pollen presentation common; exotestal cells with perforations[?].

Age. Manns et al. (2012: HPD estimates) suggest an age of (84.5-)78.5(-71.7) m.y.a. for this node.

2. [Luculia [Acranthera + Coptasapelta]]

Anthraquinones [Coptasapelta]; (raphides +).

3/53: Acranthera (35). Himalayas, China, to Malesia.

Age. Luculia diverged from [Coptosapelta + Acranthera] in the Late Cretaceous (Manns et al. 2012).

[Cinchonoideae + Ixoroideae]: shrubs or trees.

Age. B. Bremer and Eriksson (2009: stem age of this node not the crown age for the family, c.f. Fig. 1) suggested that the split of Ixoroideae and Cinchonoideae was approximately (88.7-)73.1(-58.4) m.y.a., Manns et al. (2012) give an age of (84.5-)78.5(-71.7) m.y.a., Lemaire et al. (2011b: Luculia, etc. not included) an age of (68-)60(-54) m.y.a., and Wikström et al. (2015) an age of (89-)78(-67) m.y. - but see below for uncertainty in relationships around here.

3. Cinchonoideae Rafinesque

Corynanthean and complex indole alkaloids +; (raphides + - Hillieae, Hamelieae), crystal sand +; C imbricate, valvate, (right contorted); ovules often numerous, (straight), (2, apotropous), integument ca 9 cells across; fruits usu. dry; (endosperm slight).

/1,500. Timonius (150), Hoffmannia (120), Guettarda (80), Rytigynia (70), Fadogia (45), Deppea 43). Tropical, predominantly New World.

Age. B. Bremer and Eriksson (2009) estimated that divergence within Cinchonoideae began (52.5-)38.7(-28.1) m.y.a., Manns et al. (2012: HPD estimates) gave an age of (65.6-)57.4(-50.3) m.y., and Lemaire et al. (2011b) an age of (52-)36(-24) m.y. old - but they also note "more recent stem node ages" of 26 m.y. for Cinchonoideae, all rather confusing. Antonelli et al. (2009) dated crown Cinchonoideae at some (54.6-)51.3(-47.8) m.y. and Wikström et al. (2015) suggested an age of (64-)51(-42) m.y years.

Synonymy: Catesbaeaceae Martynov, Cephalanthaceae Rafinesque, Cinchonaceae Batsch, Coutareaceae Martynov, Guettardaceae Batsch, Henriqueziaceae Bremekamp, Naucleaceae Wernham

4. Ixoroideae Rafinesque

Subshrubs to trees (herbs); iridoids common, (latex +); (calycophylls +); secondary pollen presentation common; (K lobe/lobes expanded, petal-like); C also valvate (cochleate, open, etc.), (tube with windows); (pollen in tetrads), (with buds); (placentation parietal), (stigma not bilobed - e.g. Gardenia); ovule number variable, integument ca 9 cells across; fruits often fleshy; (seed ruminate), (arillate); embryo medium (short); n = 11.

/4000: Pavetta (400), Ixora (300), Mussaenda (200), Sabicea (150), Coffea (125), Randia (100), Tricalysia (90), Wendlandia (80), Gardenia (60), Bertiera (55). Pantropical.

Age. B. Bremer and Eriksson (2009) suggested that crown-group Ixoroideae were some (73.7-)59.6(-45.7) m.y.o., Wikström et al. (2015) suggested (73-)59(-48) m.y., while Lemaire et al. (2011b) suggested ages of (60-)55(-51) m. years.

Synonymy: Coffeaceae Batsch, Dialypetalanthaceae Rizzini & Occhioni, nom. cons., Gardeniaceae Dumortier, Hameliaceae Martius, Randiaceae Martynov, Sabiceaceae Martynov

Evolution: Divergence & Distribution. For other dates in Rubiaceae, especially Spermacoceae, see Neupane et al. (2017.

A number of studies have discussed the evolution of Rubiaceae, see e.g. Bremer and Eriksson (2009) and Wikström et al. (2015: many dates). Antonelli et al. (2009) thought that Rubiaceae had a boreo-tropical origin and had moved into South America from the Old World via a North Atlantic land bridge; they also date divergences within the South American Cinchonoideae, especially within Isertieae and Cinchoneae. Manns et al. (2012), however, suggested that Ixoroideae and Cinchonoideae originated in South America ca 78.5 m.y.a., with substantial subsequent long distance dispersal - not so much by land bridges - of taxa with both wind- and animal-dipersed seeds. In particular, the palaeotropical [Hymenodictyeae + Naucleeae] probably moved there from the New World in the Eocene (Manns et al. 2012). Plants involved in long-distance dispersal seem often to have had drupaceous fruits (B. Bremer & Eriksson 1992 see also Willis et al. 2014). However, a clade of Malagasy dry-fruited Spermacoceae including Astiella (it is sister to a clade including Houstonia) may have moved there from the New World during the Oligocene, and the whole tribe is largely distylous, normally not conducive to long distance dispersal (Janssens et al. 2015). Tosh (2009) summarized biogeographical studies on Madagascan Rubiaceae

The minimum divergence time of Rubieae has been dated to (37.6-)28.6(-20.2) m.y.a. (Bremer & Eriksson 2009) with the Old World as a possible place of origin (Soza & Olmstead 2010a), although Graham (2009) suggested that Galium is known from rocks at least 55 m.y. old. Coprosma, with around 110 species, may have originated in New Zealand (or perhaps New Guinea) a mere 15-10 m.y.a., whence it was dispersed by animals perhaps some 16 times widely across the Pacific; it seems to have arrived twice in Hawaii, and multiple dispersal events to the one island are common here (Cantley & Keeley 2012; Cantley et al. 2014). Woodiness may have evolved three time in Spermacoceae in tropical uplands (Neupane et al. 2017). Looking at relationships in the pantropical Lasiantheae, Smedmark et al. (2014) emphasized how difficult it was to reconstruct biogeographical events if more than one resolution was allowed for nodes whose support was weak - not too much could be said. Indeed.

Psychotria s.l. is a very large genus of small to smallish shrubby plants that forms species swarms in the lowland tropics. It is divided up into largely Old and New World clades; the latter are included in Palicourea (Taylor 2017 for references). In the Old World there are 250+ species of species of Psychotria s.l. throughout the New Guinea/Pacific area (Andersson 2002; Nepokroeff et al. 2003: Hawaiian radiation - note that these two papers have different taxonomies; Barrabé et al. 2013; esp. Razafimandimbison et al. 2014 and references; Lim & Marshall 2017: diversity still increasing, even on old islands). The genus is abundant throughout Malesia (Nepokroeff et al. 1999; Andersson 2002), and includes the ant plants Myrmecodia, Hydnophytum and relatives (see also below); Squamellaria, also = Psychotria s.l., diversified on islands in the southwestern Pacific within the last 12 m.y. or so (Chomicki & Renner 2016a). Psychotria in New Caledonia, with some 85 species, represents another major radiation (Barrabé et al. 2013). Interestingly, its relationships are not with the Pacific Psychotria, most New Caledonian species belonging to a clade that has diversified there within the last ca 7 m.y. and is sister to an Australian clade (Barrabé et al. 2013, q.v. for many dates). In a clade of New World Psychotria (= subgenus Psychotria) older species tend to occupy larger areas than younger species (Paul et al. 2009); c.f. J. C. Willis's "age and area" hypothesis (e.g. Willis 1922), but the conceptual baggage is presumably very different in the former. Some 20 species of Psychotris grow on Barro Colorado Island in Panama, and species growing together there were more closely related than expected by chance, furthermore, the hydraulic traits studied were conserved phylogenetically (Sedio et al. 2012). Along the same lines, Sedio et al. (2013) examined the movement of Palicourea and Psychotria in the New World around about the time of the biotic interchange between North and South America (there dated to ca 3 m.y.a.) and noted that the ecological preferences of taxa that moved did not change, and that in Central America in particular the ecological diversity of these genera was increased by immigrants from South America with ecological preferences other than those of the natives.

Vincentini (2016) discusses diversification in Pagamea, one of the more prominent clades that has diversified largely on white sand in South America. See Nowak et al. (2012) for the biogeography of Coffea, which has gametophytic self incompatility, even on Mauritius. The initial colonization of that island is likely to have involved at least four, probably 14 or more seeds - and thus 2-7 fruits - arriving more or less simultaneously (Nowak et al. 2014); Coffea probably moved from Africa to Madagascar (Hamon et al. 206).

Endress (2011a) thought that the inferior ovary of Rubiaceae might be a key innovation.

Ecology & Physiology. Rubiaceae are not uncommonly epiphytic, and they represent an appreciable component of the woody epiphytic flora in the tropics (see also Ericaceae-Vaccinioideae-Vaccinieae). CAM photosynthesis has recently been detected in some species of the epiphytic and myrmecophytic Squamellaria (both = Psychotria s.l.) from Oceania (Chomicki & Renner 2016a). Indeed, in the Sout-East Asian - West Pacific region there has been considerable diversification of myrmecophytic Rubiaceae (see below), and genera like Squamellaria and Myrmecodia (both = Psychotia s.l.) are commonly found in ant gardens - assemblages of plants on trees that are the result of activities of the ants and which may have evolved up to (7.8-)5.8(-3.8) m.y.a. (Chomicki et al. 2017).

Rubiaceae are an important component of the understory vegetation of tropical forests in both Malesia and the New World. Thus they are the fourth most speciose tree family in plots from throughout the Amazonian forests, but they have very few of the larger trees, being represented by only of the 277 species that make up half the stems 10 cm or more d.b.h. in those forests (ter Steege et al. 2013).

Razafimandimbison et al. (2012) looked at the evolution of growth habit in Morindeae; the liane habit is plesiomorphic there (ca 100 species in the Old World), with independent evolution of the self-supporting habit, perhaps connected with the diversification of the clade in the neotropics. Rowe and Speck (2015) discuss the biomechanics of climbing in Galium aparine.

Pollination Biology & Seed Dispersal. Many Rubiaceae have rather small flowers, but they are often more or less closely aggregated, and Claßen-Bockhoff (1996a) has surveyed the more flower-like inflorescences that are quite common in the family. Taxa like Cephalanthus and many Morindeae and Naucleeae have flowers aggregated into spherical heads, and in Morindeae there has been evolution of simple fruits in which the individual fruis are fused from multiple fruits (Razafimandimbison et al. 2012). Cephaelis (= Palicourea: Rubioideae) has a condensed inflorescence immediately subtended by paired and coloured inflorescence bracts, while large, coloured calyces (calycophylls) are particularly common in Ixoroideae and help to attract the pollinator. The Old World Mussaenda is an example with large petal-like calyx lobes usually occurring singly on a few flowers in the quite lax inflorescence (the genus may be polyphyletic - see Alejandro et al. 2005) - and see also Nematostylis, while in the New World Warsewiczia has similarly conspicuous individual sepals - and see also Wittmackanthus, Calycophyllum, etc..

In some species of Spermacoce (Rubioideae) the apices of the corolla lobes are incurved and extensively modified, and pollination is explosive (Vaes et al. 2006); palynological variation here is extreme, being almost equivalent to that in the whole of the rest of the family (Dessein et al. 2002). Explosive pollination is also known from Posoquerieae (Ixoroideae), pollen being catapulted onto the pollinating insect; the flowers are monosymmetric and may be inverted (Delprete 2009; Cortés-B. & Motley 2015). Secondary pollen presentation is notably common in Cinchonoideae (Nilsson et al. 1990; Puff et al. 1996; de Block & Igersheim 2001), but it is also quite common in Ixoroideae (e.g. Vanguerieae - Tilney et al. 2011; see also Kainulainen et al. 2013); pollen is presented on tips of the styles. Rubiaceae are noted for the frequency of distyly in the family - for instence, hundreds of Rubioideae, and overall, perhaps half the whole family (Bir Bahadur 1968; Robbrecht 1988) are involved, although taxa with secondary pollen presentation tend not to be involved and there have been several reversals to homostyly (Ferrero et al. 2012). Anderson (1973) suggested that heterostyly had evolved several times from protandrous self-compatible ancestors. Dioecy occurs in a number of neotropical Gardenieae (Ixoroideae) like Randia that have large fleshy fruits (C. Taylor, pers. comm.). In Vanguerieae there are apparent reversals to hermaphroditism (Razafimandimbison et al. 2009), and in New World Galium there may have been reversals to polygamy (Soza & Olmstead 2010b).

In South East Asia Rubiaceae are important food resouces for frugivores because they produce crops of sugar-rich fruits more or less aseasonally (Leighton & Leighton 1983), indeed, they are the most important euasterid food resource for smaller unspecialized avian frugivores in general (Snow 1981). Myrmecochory occurs in a number of Malesian-Pacific ant-inhabited Rubioideae-Hydnophytinae (Chomicki & Renner 2016b, see also below). Although Gentianales as a whole have small seeds, those of Henriquezia are up to 8 cm in diameter (Cortés-B. & Motley 2015).

Within Rubiaceae there may be a correlation between fruit types, plant habit, and diversification. Thus clades that are shrubs or trees and in which winged seeds are apomorphic, shrubs with animal-dispersed fruits, and herbs with abiotic dispersal (but not winged seeds), are all notably speciose (Eriksson & Bremer 1991; B. Bremer & Eriksson 1992). Fleshy fruits may have evolved about twelve times in the family, especially during the Eocene-Oligocene period (B. Bremer & Eriksson 1992), although this figure is likely to be an underestimate, fleshy fruits having evolved at least four times in a New World clade of Galium alone (Soza & Olmstead 2010b, q.v. for other fruit morphologies there); for the evolution of schizocarpous fruits in Psychotria, see Razafimandimbison et al. 2014). In cases of apparent long-distance dispersal in the family, the plants involved seem often to have had drupaceous fruits (B. Bremer & Eriksson 1992).

Plant-Animal Interactions. Rubiaceae are not often eaten by caterpillar larvae of butterflies (Ehrlich & Raven 1964), although some sphingids (Semanophorae) do prefer members of the family (Forbes 1956).

Some 140 species of Rubiaceae in 22 genera are myrmecophytes (Razafimandimbison et al. 2005). Myrmecodia, Hydnophytum and related Malesian genera (Psychotrieae-Hydnophytinae, = Psychotria s.l.) are highly modified epiphytic ant plants, and are the largest such clade (Chomicki & Renner 2015, 2017). All told, 82/105 species of this group are myrmecophytes, and crown-group Hydnophytinae have been dated to around 13.7 m.y.a. (Chomicki & Renner 2015: Fig. S7, 17 species of Hydnophytinae in tree, 2016), or perhaps (9.3-)6.3(-3.3) m.y.a. - and for other rubiaceous clades involved, ages are younger (Chomicki & Renner 2017a; Chomicki et al. 2017). The ants, whether specialists or generalists, and also - mainly at higher altitudes - other organisms such as frogs, live in chambers in the grossly swollen stem (hypocotyl) base (Chomicki & Renner 2017a). Material brought in by the ants is stored in chambers with warty walls and nutrients from this material and from ant excreta are taken up by the plant. Some species have more or less branched spines arising from the root, stem, inflorescence, and even the torn and eaten surfaces of the leaves (Huxley 1978; Jebb 1991; Huxley & Jebb 1991 for the taxonomy of the group). Some, but not all, species of Fijian Squamellaria (= Psychotria s.l.) have a close association with the ant Phildris nagasau, and the floral disc keeps on producing nectar for ten or more days after anthesis, the ants, but not other insects, being able to take this nectar from the plant; fruit development does not begin until after nectar secretion stops (Chomicki et al. 2016a). Furthermore, P. nagasau disperses the seeds of these Squamellaria, puts them in cracks in the trunk of the host trees, and even fertilizes the seedings (by defaecating into the hypocotylar domatium?) before they are occupied by the ant; the Squamellaria seedlings develop a long hypocotyl which enables them to grow out of the cracks in which they have been placed more easily (Chomicki & Renner 2016b). Close associations with ants have arisen several other times in Rubiaceae. Thus there are several myrmecophytic Naucleeae, the ants - a variety of species are involved (Razafimandimbison et al. 2005) - living in hollowed stems in plants with a much more "normal" appearance than that of many Hydnophytinae. Interestingly, some of these myrmecophytic clades have diversified notably slowly and/or have very limited distributions, with about 18/68 species being myrmecophytes and about three origins of the habit (Razafimandibison et al. 2005). The myrmecophytes are estimated to be ca 16 m.y.o. or much younger (Chomicki & Renner 2015: fig. S11), but the sampling, focussed on myrmecophytes, is slight. In the western Amazon, Duroia hirsuta is sometimes associated with the ant Myrmelachista schumanni which forms "devil's gardens" by poisoning other surrounding vegetation with formic acid (Salas-Lopez et al. 2016 and references).

Bacterial/Fungal Associations. Bacterial leaf nodules are known from some African species of Psychotria (Rubioideae), and their presence is correlated with development of distinctive colleters (Lersten 1974 and references). Leaf nodulation seems to have originated in mainland taxa which then moved to Madagascar and the Comoros independently, but not to the Mascarenes; nodulation has sometimes been lost, and also independently acquired in the Malagasy P. bullata (Razafimandimbison et al. 2014). Bacteria of the ß-proteobacterium Burkholderia have been isolated from the nodules (van Oevelen et al. 2004). Some species of Burkholderia are nitrogen-fixing symbionts in the root nodules of Fabaceae-Faboideae, but nitrogen fixation has not been detected in Psychotria (Miller 1990). There are about 440 species of Pavetta and Sericanthe with leaf nodules; there transmissal of Burkholderia is largely vertical, although there is also horizontal movement, and the association is not of very long standing (Lemaire et al. 2011b). Members of two groups of Burkholderia also grow free in the leaf between mesophyll cells in some African Vanguerieae (Ixoroideae), an association that seems largely specific from the plant's point of view but not from that of the bacteria (Verstraete et al. 2013a, b). This association seems to have evolved three times, although any benefits to the partners are unclear (Verstraete et al. 2013b), all told, some 150 species of Vanguerieae may be involved.

Vegetative Variation. Although most Rubiaceae can be recognised by a distinctive combination of vegetative characters (see above), vegetative variation in the family is quite extensive, even apart from the remarkable morphologies of the myrmecophytic taxa just mentioned. Herbaceousness is prevalent in Rubioideae, but some Spermacoceae may be secondarily woody, and Knoxeae are both primarily and secondarily woody (Lens et al. 2009a, b). Genipa and Posoqueria have a deeply lobed lamina; "latex" is not uncommon. Anisophylly is well known in the family, occurring in herbaceous taxa like Theligonum and Argostemma, where it is especially marked in taxa like A. humilis.

Rubiaceae are vegetatively very distinctive - opposite entire leaves + interpetiolar stipules will do it. That being said, stipule morphology and position shows considerable variation; there are sometimes two pairs of stipules, one more or less intrapetiolar, the other interpetiolar. The leaves may be strongly lobed, anisophyllous, and even "alternate" - 2-ranked. Most taxa have 1:1 nodal anatomy; branches separate from the single trace and form a vascular collar around the stem from which the stipular bundles diverge (Majumdar & Pal 1958). However, a number of genera are trilacunar (Neubauer 1981; Robbrecht & Puff 1986); this does not seem to correlate with phylogeny. In angiosperms, unilacunar nodes are unusual in taxa with stipules, trilacunar nodes being the norm (Sinnott & Bailey 1914). For more on interpetiolar stipules, seee Mitra (1948).

The exact nature of the "whorled leaves" of Galium has been a matter of some dispute. Soza and Olmstead (2010a) suggested that the basic condition in Rubieae was to have six leaves per whorl (c.f. L.-E Yang et al. 2015), although there was frequent evolution of four-membered whorls (and even reversal to six again). Galium and related genera lack distinct stipules, but there are only two opposite branches per node, suggesting that the basic construction of the plant is of paired, opposite leaves; this is confirmed by the pattern of vascularization in most species (e.g. Neubauer 1981), including that in genera like Phuopsis (pers. obs.) - a 1:1 node with girdling traces. However, taxa like Galium rubioides have four large leaves at the node all of which are directly vascularized from the stele (Rutishauser 1999); this is likely to be a derived condition (Soza & Olmstead 2010a). Leaves and stipules may develop from different primordia (e.g. Pötter & Klopfer 1987), and it has even been suggested that "leaf-like stipules are independent structures, not part of the leaf" (Soza & Olmstead 2010a: p. 768). At the same time species like G. paradoxa sometimes have opposite leaves with paired, interpetiolar stipules - and there is similar variation in the unrelated Limnosipanea (C. Taylor, pers. comm.; = Galium s.l.) and also in Rubia (L.-E Yang et al. 2015).

Colleters are common in the family (e.g. Lersten 1974; Miguel et al. 2010 and references). However, Henriquezia and Platycarpum lack colleters, although they have glands on the leaves that may secrete nectar (Cortés-B. & Motley 2015).

Genes & Genomes. Molecular evolution in the herbaceous Rubioideae seems to be speeded up compared to that in the woody members (Rydin et al. 2009b); note the laggard woody Dunnia within the herbaceous clade!

Chemistry, Morphology, etc. For cyclotide proteins, found in Oldenlandia, Psychotria, and relatives in Rubioideae, see Gruber et al. (2008) and Koehlbach et al. (2013). Petiole anatomy is variable, and although the vascular bundles are often more or less arcuate, in some Ixoroideae they are annular (Martínez-Cabrera et al. (2009).

In some taxa the calyx begins to develop after the corolla, but this is only when the calyx lobes are much reduced; the calyx tube does develop later (de Block & Vrijdaghs 2013). Floral - especially corolla - development has been carefully analysed in Spermacoceae, where the corolla may be fenestrate; corolla tubes are variously produced from an annular intercalary meristem (a stamen-corolla tube), an intercalary meristem in a different position produces a corolla tube sensu stricto, or corolla lobes may fuse postgenitally, and all in all it is difficult to distinguished between early and late corolla tube development (Vrijdaghs et al. 2015). Taxa like the sister genera Gaertnera (see Malcomber 2002) and Pagamea (Vincentini 2016) have secondarily superior ovaries (Igersheim et al. 1994). A few Rubiaceae like Theligonum and Dialypetalanthus have more than twice the number of stamens as perianth/sepals/petals (e.g. Endress 2003a; see also euasterids). For pollen variation in the paraphyletic Spermacoce, see Dessein et al. (2005b). There is considerable variation in ovule morphology and development (Maheshwari 1950; de Toni & Mariath 2008, 2010; Figueiredo et al. 2013). Ronse Decraene and Smets (2000) discuss floral development in the family, emphasizing variation in the relative development of a stamen-corolla tube with a common meristem and a corolla tube s.s.; filaments may fuse postgenitally with the corolla tube proper. There is considerable variation in the pattern of thickening of the exotestal cells; as might be expected, taxa with drupaceous fruits have a less well developed exotesta (Robbrecht & Puff 1986).

For additional information on Rubiaceae, see Verdcourt (1958), Robbrecht (1988, 1993), Robbrecht et al. (1996), Delprete (2004) and Rogers (2005), all general, for chemistry, see Martins and Nunez (2015: >450 references, to be digested), for alkaloids, see Aniszewski (2007) and Berger et al. (2012), for Al and Si accumulation, see Jansen et al. (2002a, 2003), for toxic monofluoracetates, see Lee et al. (2012), and for the chemistry of Psychotria and relatives, see Berger (2012); also see Koek-Noorman & Hogeweg (1974), Koek-Noorman (1977: group I- and II-type woods), Martínez-Cabrera et al. (2010), León H. (2013) and Martínez-Cabrera et al. 2015), all wood anatomy, Rutishauser (1984: stipules), Miguel et al. (2010), Tresmondi et al. (2015) and Lopes-Mattos et al. (2015), all colleters, Gamalei et al. (2008: phloem), and Lersten and Horner (2011: calcium oxalate crystal morphology in Naucleeae [Cinchonoideae], interesting variation). See also Weberling (1977: inflorescences), Rogers (1984: Gleasonia, etc.), Puff et al. (1993a: pollen, fruits in Mussaenda et al., 1993b, much detail about Schradereae), Huysmans et al. (1997: Cinchonioideae), Vinckier et al. (2000: Ixoroideae) and Verstraete et al. (2011), all orbicules, D'Hondt et al. (2004), Dessein et al. (2005a) and Verellen et al. (2007), pollen, Rakotonasolo and Davis (2006: some odd placentation types), Lloyd (1899, 1902: embryology), Fagerlind (1937: embryology and much else), and Takhtajan (2013: esp. seeds). For floral morphology, see Igersheim (1993b: Strumpfia) and Martínez-Cabrera et al. (2013: Hamelieae, etc.) and for chromosomes of Rubioideae, see Kiehn (2010).

Phylogeny. B. Bremer (2009) summarizes phylogenetic work on the family (see also Bremer 1996b). The basic phylogenetic structure is [Rubioideae [[Luculia [Acranthera + Coptasapelta]] [Cinchonoideae + Ixoroideae]] (see B. Bremer 1995, 1999; Rova et al. 2002; Robbrecht & Manen 2006; Rydin et al. 2009a; etc.). The clade of Luculia and Coptosapelta - and now Acranthera - seems moderately well supported. However, Bremer and Eriksson (2009) suggested that the three might not form a single clade, and while they do form a clade in Manns et al. (2012), it is sister to Rubioideae. Wikström et al. (2015: no Acranthera) found Luculia and Coptasapelta successively sister to the subfamily. In L.-L. Yang et al. (2016) the basal structure in the family was [[Acranthera + Coptasapelta] [Rubioideae [Luculia [Cinchonoideae + Ixoroideae]]]], or some other variation on the theme, although support was very weak, while in Z.-D. Chen et al. (2016) relationships were [[[Rubioideae [Acranthera + Coptasapelta]] Luculia] [Cinchonoideae + Ixoroideae]], but with weak support at the base of the Rubioideae side of the tree. Refulio-Rodriguez and Olmstead (2014) found moderate support for the placement of Luculia as sister to the other four Rubiaceae they examined (these included representatives of all three subfamilies).

Luculia and Coptasapelta are not close morphologically: As Robbrecht and Manen (2006) emphasized, the two differ in having, as in Coptosapelta, or not, as in Luculia, raphides, accumulating (or not) aluminium, having T-shaped hairs (not), pororate, acolumellate (tricolporate) pollen grains, and distyly (secondary pollen presentation) (Verellen et al. 2004; for pollen presentation, see Puff et al. 1996). Although Acranthera may be sister to Coptasapelta (see also Bremer & Eriksson 2009), these two also have little morphologically in common (Rydin et al. 2009a). Thus assigning polarity to many features in the family becomes rather tricky.

Within Rubioideae, Opiorrhiza has the atpB promoter region that is lacking in other Rubioideae (Manen & Natali 1996; Natali et al. 1996) and was thought to be sister to the rest of the subfamily. Rydin et al. (2009a) found it was close to Urophylleae, mainly because of support from ITS, not chloroplast genes, and relationships between major clades in Urophylleae are clarified by Smedmark and Bremer (2011: note, species-level relationships unclear). Sister to the whole of Rubioideae, and with strong support, is the monotypic African genus Colletoecema (Piesschart et al. 2000: near basal, actual position uncertain; esp. Rydin et al. 2009a; L.-L. Yang et al. 2016); does it have an atpB promoter region? Rydin et al. (2008) discuss the placement of some other small and little-kmown genera of Rubioideae; they considerably affect our understanding of the evolution and diversification of the clade. Smedmark et al. (2015) examined relationships within the pantropical Lasiantheae.

The relationships and limits of Psychotria and its relatives pose problems. The Psychotria and Palicourea complexes are sister taxa. The former, which often has caducous stipules, is largely divided into Old and New World clades, while the latter includes some species of Psychotria (Taylor 2017 and references). A Malesian-Pacific clade of Psychotria includes myrmecophytes as well as genera like Amaracarpus (Nepokroeff et al. 1999; Andersson 2002: the optimisation of marginal preformed germination slits on the pyrenes is questionable; Razafimandimbison et al. 2008); Cephaelis groups with Palicourea, and overall there is considerable geographical signal in the clades. Barrabé et al. (2012) focused on relationships of a clade of the Palicourea group, the Malesian-Pacific-American Margaritopsis. Morinda (Morindeae), with its distinctive capitate inflorescences and compound fruits, is in fact polyphyletic (Razafimandimbison et al. 2009b, 2012).

The Spermacoceae alliance (e.g. L.-L. Yang et al. 2016) includes about nine tribes. Relationships within the ca 1000 species of Spermacoceae are a major problem. Kårehed et al. (2008) investigated the phylogeny of Spermacoceae; they suggested that Hedyotis was to be resticted to Asian taxa. Wikström et al. (2013) is another important step forwards here, and for further studies in Spermacoceae, see Groeninckx et al. (2009a, esp. 2009b), Rydin et al. (2009b), Guo et al. (2013: Asian taxa) and Neupane et al. (2015: whole Asia/Pacific area). Both morphology and molecular data strongly support the monophyly of Rubieae (Rogers 2005 for literature). There is now considerable phylogenetic resolution within the tribe, with relationships between seven strongly-supported (both bootstrap and posterior probabilities) major clades themselves being well supported; the basic structure in the Galium area is [many species of Galium [4 clades made up mostly of generic segregates, support could be stronger [many species of Galium]]] (Soza & Olmstead 2010a, also 2010b for New World Galium; see also Manen & Natali 1995; Manen et al. 1994; Natali et al. 1996). De Toni and Mariath (2011) found that flowers and fruits suggested that Galium and Relbunium were sister taxa and both worthy of generic status. However, Soza and Olmstead (2010b) noted that the fleshy fruits of Relbunium were distinctive (but not unique) in Galium, and the Relbunium group was embedded in a larger South American clade that is firmly part of Galium. Asperula, within which Sherardia is nested, is also part of this problem (Gargiulo et al. 2015), while L.-E Yang et al. (2015) looked at relationships within Rubia - Didymaea is its sister clade, and the South African R. horrida was sister to a large eastern Asian clade.Ginter et al. (2015) discussed relationships around Argostemma, Argostemmateae, also part of this whole complex.

For further information on the phylogeny of Rubioideae, see Andersson and Rova (1999), B. Bremer and Manen (2000: phylogeny and classification), Backlund et al. (2007), Wikström et al. (2015: note basal clades), Kårehed and Bremer (2007: Knoxieae), Smedmark (2008: Urophylleae), Razafimandimbison et al. (2008: relationships around Psychotrieae, many-seeded carpels evolve from one-seeded carpels in Schradereae, esp. 2014) and L.-L. Yang et al. (2016).

For phylogenetic relationhips within Cinchonoideae, see Andreasen and Bremer (1996), Rydin et al. (2009), and especially Manns et al. (2012) and Manns and Bremer (2010); the latter recognise nine tribes within the subfamily, all of which are strongly supported as being monophyletic, however, some of the relationships between groups of tribes are as yet poorly resolved (Manns & Bremer 2010; see also Paudyal et al. 2104). For relationships within these tribes, see Manns and Bremer (2010) and Manns et al. (2012), also, within Vanguerieae, see Lantz and Bremer (2005) and references and Razafimandimbison et al. (2009). For relationships in Sabiceeae, see Khan et al. (2008). [Naucleeae + Hymenodictyeae] are a well supported clade sister to the only moderately (jacknife) supported remainder of Cinchonoideae (Andersson & Antonelli 2005: Luculia and Coptasapelta excepted; L.-L. Yang et al. 2016). See also Razafimandimbison & Bremer (2002), Razafimandimbison et al. 2004, and especially Löfstrand et al. (2014) for Naucleeae and Hymenodictyeae, Stranczinger et al. (2014) make preliminary suggestions about relationships in Hamelieae, and L.-L. Yang et al. (2016) discuss relationships in Chinese members of the subfamily.

Ixoroideae. The six-plastid gene study of Kainulainen et al. (2013: Dialypetalanthus not included) provided substantial support for relationships throughout Ixoroideae, although those in the "basal" Condamineeae-Mussaendeae area remained somewhat unclear. However, few deep relationships in the subfamily had strong support - nor did the subfamily itself - in the study by L.-L. Yang et al. (2016), which focused on its Chinese representatives. Condamineeae as circumscribed by Kainulainen et al. (2010) are very heterogeneous and include Mastixiodendron, the morphologically even more distinctive Dialypetalanthus (see also Feng et al. 2000), several genera with calycophylls, etc.. For the circumscription of Coffeeae, see A. Davis et al. (2007), and Maurin et al. (2007) and Nowak et al. (2012) and Hamon et al. (2017) for the phylogeny of Coffea itself. There are four main clades witin Pavetteae, and Tarenna in particular is polyphyletc, Lepactina paraphyletic (de Block et al 2015). Razafimandimbison et al. (2011) found that at the base of the clade encompassing the ca 1100 species of Vanguerieae there were successively four monogeneric clades (three in Kainulainen et al. 2013, Glionettia unplaced). See Razafimandimbison et al. (2009a) for the phylogeny of dioecious Vanguerieae. Relationships within the old Gardenieae are becoming clarified, and Pavetteae, Gardenieae, and two small tribes may form a clade, although without bootstrap support (Mouly et al. 2014: chloroplast data). The Madagascan Melanoxerus (Gardenieae) links with African taxa in plastid and ribosomal analyses, but with neotropical taxa in nuclear gene analyses (Kainulainen & Bremer 2014). Alejandro et al. (2011) look at relationships within Octotropideae, while Zemagho et al. (2016) clarify relationships in Sabiceeae. Ixora (Ixoridinae) is paraphyletic (Mouly et al. 2009a, b, see also Andreasen & Bremer 2000; Tosh et al. 2013: Afro-Madagascan species). Tosh et al. (2009) have adjusted the limits of the African Tricalysia (see also Tosh 2009), Cortés-B. et al. (2009) looked at Retiniphylleae and Kainulainen et al. (2009) at Alberteae. Sipanea and Posoqueria form a basal clade (Razafimandimbison et al. 2011; Mouly et al. 2014); Cortés-B. and Motley (2015) discussed relationships around Henriquezia, Sipanea and Posoqueria, although how the extensive variation in flower and fruit in particular relates to living on the nutrient-poor soils of the Guayana region is not clear.

Two genera are particularly odd morphologically:

Classification. Robbrecht and Manen (2006) and B. Bremer (2009) should be consulted for a detailed discussion on taxon limits, formal classification, and the like. Manns and Bremer (2010) provide a tribal classification of Cinchonoideae and assign nearly all genera to those tribes, at least provisionally (see also Paudyal et al. 2104). There is a tribal classification of Ixoroideae in Kainulainen et al. (2013) where genera in 21 of the 24 tribes are enumerated; one genus (Glionettia) is unplaced. See Govaerts et al. (2013) for a World Checklist of Rubiaceae.

Bremer (2009) noted that of the ca 611 genera in the family, 1/3 were monotypic - but others are very large and are turning out to be paraphyletic. Not surprisingly, generic limits are problematic in a number of places, indeed, if preserving the names of these small genera seems desirable, then wholesale dismemberment of larger genera and ever more small genera will be the logical if unfortunate result. Within Rubieae, the circumscriptions of both Asperula and Galium are currently a mess (Soza & Olmstead 2010a). In Galium in particular, fruit morphology is a poor indicator of sectional relationships (Soza & Olmstead 2010b; see also Abdel Khalik et al. 2009). Enhrendorfer et al. (2014) sketch out a possible taxonomic solution allowing paraphyly of genera (see also Kästner & Ehrendorfer 2016: pp. 56-58), but in the generic synonymy here a broad circumscription for Galium is suggested, largely following the phylogeny in Sosa and Olmstead (2010a). Spermacoceae are very difficult with both considerable lumping and considerable splitting having occurred in the past. Oldenlandia appears to be wildly polyphyletic, and Spermacoce very paraphyletic (Kårehed et al. 2008; Wikström et al. 2013), and new genera are being described in the context of local phylogenetic analyses (Groeninckx et al. 2010a, b). Thus X. Guo et al. (2013) described three new genera from the Asian part of the Spermacoce complex, but another 10-17 names (several do already exist) will then be needed to describe just this part of the tree. Neupane et al. (2015) summarize generic relatiomnships in the whole Hedyotis-Oldenlandia area. For generic limits in Urophylleae, see Smedmark and Bremer (2011: nine of Bremekamp's small genera still unsampled). Generic limits around the polyphyletic Morinda have been adjusted (Razafimandimbison et al. 2009). A Pacific-Malesian clade of Psychotria also includes myrmecophytes like Myrmecodia and Hydnophytum as well as genera like Amaracarpus (Andersson 2002); Andersson (2002) seemed inclined to split the clade, while e.g. Nepokroeff et al. (1999) and particularly Razafimandimbison et al. (2014) would include them in Psychotria s.l., which seems preferable to me. Taylor (2017 and references) is in the process of making the nomenclatural changes needed because of the expansion of Palicourea.

In Cinchonoideae, the limits of Ixora have been clarified (Mouly et al. 2009a, b). Generic and tribal limits are diffficult around Rondeletieae and Guettardeae (Rova et al. 2009); Guettarda itself is polyphyletic (Achille et al. 2006). See Löfstrand et al. (2014) for a discussion on generic limits in Naucleeae. In Ixoroideae Coffea is to include Psilanthus (Maurin et al. 2007), while the composition of Sabiceae, and a subgeneric classification of Sabicea itself, is to be found in Zemagho et al. (2016).

Pavetta (400), Ixora (300), Mussaenda (200), Sabicea (150), Coffea (125), Randia (100), Tricalysia (90), Wendlandia (80), Gardenia (60), Bertiera (55).

Previous Relationships. Rizzini and Occhioni (1949) were sure Dialypetalanthaceae were in Myrtales, while Cronquist (1981) placed them adjacent to Pittosporaceae in his Rosales, but Theligonaceae were at least placed in Rubiales. Both families were kept separate by Takhtajan (1997) and were included in his Rubiales.

Thanks. I am grateful to Elmar Robbrecht for help with the synonymy and to Charlotte Taylor for many useful comments.

[[Loganiaceae + Gelsemiaceae] [Gentianaceae + Apocynaceae]]: route I secoiridoids +; internal phloem + [bicollateral vascular bundles]; K valvate or imbricate; C tube formation late; syncarpy postgenital; testa with anticlinal walls thickened.

Age. Bell et al. (2010) give an age of (69-)61, 57(-47) m.y. and Magallón et al. (2015) around 60 m.y. for this clade, but see relationships within it; (93-)73(-49) m.y.a. are the ages in Wikström et al. (2015).

[Loganiaceae + Gelsemiaceae]: quercetin, kaempferol +; C imbricate; endosperm horny [starchy/hemicellulosic].

Age. (87-)64(-39) m.y.a. are the ages for this clade in Wikström et al. (2015), ca 52.3 m.y. in Tank et al. (2015: Table S2), and (67.5-)41.8(-18.3) m.y. in Tank and Olmstead (2017).

Phylogeny. Backlund et al. (2000) noted that C17 indole alkaloids, the number of tapetum layers, and cytology supported the relationship [Gelsemiaceae + Apocynaceae], but that the presence of quercetin and kaempferol, imbricate corolla, and horny (starchy) endosperm might support a close relationship between Gelsemiaceae and Loganiaceae.

LOGANIACEAE Martius, nom. cons.   Back to Gentianales


Annual herbs to shrubs or lianes; tryptophane-derived alkaloids +; nodes also 3:3 (and split laterals); stomata?; lamina vernation ± flat, (secondary veins palmate), (sheathing stipule +); flowers 4- or 5-merous, (median K abaxial - Logania), (monosymmetric - Usteria); K basally connate or not, (C also valvate, contorted, quincuncial), often hairy at the mouth; (A 1, abaxial - Usteria); tapetum (amoeboid), polyploid [Strychnos]; pollen grains tricellular [?all]; nectary 0, poorly developed, or gynoecial; G collateral, (-5), often partly inferior and partly apocarpous (congenitally syncarpous), (placentae massive), (stylar fusion postgenital), styles branches +/0, stigma capitate, long-clavate, 2-lobed, or punctate; ovules (1-)many/carpel, epitropous [?always], integument 4-6 cells across; fruit a follicle, loculicidal and/or septicidal capsule, drupe or berry; (placentae fleshy - Gelsemium), (seeds embedded in pulp), seeds ruminate - Spigelia); exotestal cells papillate or hairy, ± thick-walled and lignified except outer wall; n = 10, 12, 16; seedings epigeal and phanerocotylar.

13[list]/420: Strychnos (190), Mitrasacme (55), Geniostoma (55). Pantropical, esp. Australia and New Caledonia (map: from Leenhouts 1962; van Steenis & van Balgooy 1966; Leeuwenberg 1969). [Photo - Flower, Fruit]

Age. The clade [Spig. + Strych.] is some (70.8-)44.7(-18.3) m.y.o. (Tank & Olmstead 2017).

Chemistry, Morphology, etc. The wood of Strychnos has included phloem; the plant has branch tendrils.

Colporate pollen without lateral extensions at the endocolpus is reported to be a character restricted (in this group) to Strychnos and its immediate relatives. The ovules of Mitrasacme have an endothelium and the endosperm is "intermediate" in development, while Mitreola oldenlandioides has straight ovules and cellular endosperm (Reddy et al. 1999). The herbaceous Spigelia is distinctive. Its leaves are often pseudoverticillate; the inflorescence is a cincinnus; and its fruit is a septicidal+loculicidal capsule, the valves all falling off.

For information, see Leeuwenberg (1980: general), Aniszewski (2007: alkaloids), Keller (1996: "stipules"), Hasselberg (1937: nodes and stipules), Dahlgren (1922), Bendre (1975) and Maheswari Devi and Lakshminarayana (1960: ?Strychnos with an endothelium), all embryology, and, Hakki (1998: Usteria).

Phylogeny. L.-L. Yang et al. (2016) found the relationships [Antonieae [Spigelieae embedded in Strychneae + Loagnieae]], with quite good support. For relationships in Loganieae, see Gibbons et al. (2012); generic limits will have to be adjusted.

Synonymy: Antoniaceae Hutchinson, Gardneriaceae Perleb, Geniostomataceae L. Struwe & V. Albert, Spigeliaceae Berchtold & J. Presl, Strychnaceae Perleb

GELSEMIACEAE L. Struwe & V. Albert   Back to Gentianales


Trees, shrubs or lianes; camptothecin-type alkaloids +; true tracheids +; stomata?; (leaves spiral), (margins serrate), (stipules 2, interpetiolar or short sheathing); (flowers single); flowers heterostylous (not); A latrorse (extrorse - Gelsemium); pollen pores with distinct lateral extensions [?level], surface striate to reticulate; nectary +, ?position; (G stipitate - Pteleocarpa), style twice (once) branched, stigma puctate (capitate); (ovules 2/carpel); fruit a loculicidal and/or septicidal capsule, (muricate), (1-seeded samara - Pteleocarpa), K usu persistent; seeds winged or hairy, flattened, or rugose, (not); testa?; n = 8, 10.

2[list]/11. ± Pantropical (map: from Leeuwenberg 1961; van Steenis & van Balgooy 1966; Sobral & Rossi 2003). [Photo - Gelsemium Collection © M. Dirr, Flower (Pin), Flower (Thrum).]

Age. Crown-group Gelsemiaceae are (61.7-)36.8(-13.9) m.y.o. (Tank & Olmstead 2017).

Evolution: Divergence & Distribution. For the phylogeny and biogeography of the family (Pteleocarpa not included), see Jiao and Li (2007).

Pollination Biology and Seed Dispersal. Considerable work has been caried out on the nectar of Gelsemium, containing as it does alkaloids, to work out its effects on (potentially) pollinating bees, both adults and larvae, and what effect it might have on selfing, etc. (Irwin & Adler 2008 and references).

Chemistry, Morphology, etc. Vascular pits in Gelsemium are not vestured (Rogers 1986), those of Pteleocarpa are. The latter also has mainly apotracheal parenchyma in unilateral, uniseriate bands and fibre tracheids with bordered pits (Gottwald 1982).

How nectar is secreted in Pteleocarpa is unclear (Struwe et al. 2014).

Phylogeny. The association of Pteleocarpa with this clade is strongly supported. Refulio-Rodriguez and Olmstead (2014) suggested that it was sister to the two other genera, Struwe et al. (2014) did not place it.

Classification. Although Pteleocarpa is a distinct genus - Brummitt (2007, 2011) recognized it as a separate family - it is best included in Gelsemiaceae (see Struwe et al. 2014).

Previous Relationships. Pteleocarpa has been included in Boraginaceae-Ehretioideae, e.g. by Takhtajan (1997); the other genera are ex-Loganiaceae.

Synonymy: Pteleocarpaceae Brummitt

[Gentianaceae + Apocynaceae]: monoterpene indole alkaloids; (interxylary phloem); C contorted; postgenitally fusing carpels flat; testa multiplicative, exotestal cells with thickenings on their anticlinal walls.

Age. The age of this clade is around 62 m.y. (Naumann et al. 2013), ca 52.1 m.y. (Magallón et al. 2015), (86-)62(-39) m.y.a. (Wikström et al. 2015) or ca 48.1 m.y. (Tank et al. 2015: Table S2).

Chemistry, Morphology, etc. Gentianaceae and Apocynaceae are the only families in which postgenitally fusing carpels are flat, not plicate (Kissling et al. 2009b). Bouman and Schrier (1979) noted that exotestal cells with thickenings on their anticlinal walls are common around here; Gelsemiaceae and Loganiaceae were not mentioned.

GENTIANACEAE Jussieu, nom. cons.   Back to Gentianales


Herbs to shrubs (trees), mycorrhizal (and echlorophyllous); (plants Al-accumulators); starch 0, oligosaccharides +, tannins 0; cork?; (vessel elements with scalariform perforation plates); rays often 0; parenchyma septate; nodes 1:3 (3 or more:3 or more), (+ split laterals); mucilage cells + (0); plant glabrous; (stomata anisocytic); leaves sessile, usu. connate basally, lamina vernation variable, secondary veins ± palmate (pinnate); flowers 4-5-merous, "disc-like" structure between K and C, C right-contorted, marcescent, (tube formation intermediate), petal epidermal cells elongated and flat; A basally connate, (extrorse), (placentoids +); tapetum (amoeboid), cells uninucleate; nectary 0; G ?collateral, style often short, stigma broadly 2-lobed (capitate), wet; funicle with at best poorly developed vascular tissue, (outer epidermal cells of integument early massive), hypostase +; (antipodal cells diploid to polyploid), (multiplying, persistent); fruit a septicidal capsule, calyx often prominent; seeds small to minute; exotestal cells (± elongated), inner walls variously thickened (not), other layers ± disappear; embryo white or green; 100 bp deletion in trnL gene.

Ca 99[list]/ca 1,740 - 7 tribes below. World-wide, but especially temperate, about half the genera in South America (map: from Gillett 1963; Hultén 1958, 1971; van Steenis & van Balgooy 1966; Klackenberg 1985; Ho & Liu 2001; Struwe & Albert 2004; Kissling 2012). [Photo - Flower, Flower.]

Age. The crown age of the family may be some 50 m.y. (Y.-M. Yuan et al. 2003), (78.2-)59.5(-40) m.y. (Tank & Olmstead 2017), or (78.6-)66.2, 57.8(-47.3) m.y. (Merckx et al. 2013c); there are suggestions of an age as great as (125-)just under 100(-75) m.y. (Kissling in Struwe 2014).

Although fossils with pollen like that of Macrocarpaea are reported from the Eocene ca 45 m.y.a., their identity is questionable (Stockey & Manchester 1985; Struwe et al. 2002).

1. Saccifolieae Struwe, Thiv, V. A. Albert & Kadereit

(Echlorophyllous mycoheterotrophic herbs, associated with glomeromycotes), (shrubs); ?chemistry; extrafloral nectaries simple; (leaves spiral); flowers (heterostylous), (4-)5(-6)-merous; placentation parietal; (dust seeds +); (endosperm cellular - Voyriella), (cotyledons 0); n = 10-14.

5/19. tropical South America, Panama.

Synonymy: Saccifoliaceae Maguire & Pires

[Exaceae [Voyrieae [Chironieae [Potalieae [Helieae + Gentianeae]]]]]: ?

Age. This node was dated to some (57.4-)49.1, 48.6(-40.1) m.y. by Merckx et al. (2013c).

2. Exaceae Colla

(Echlorophyllous mycoheterotrophic herbs); (flowers monosymmetric/enantiostylous - Exacum, Orphium, obliquely monosymmetric - Exacum); (median petal adaxial); K connate or not, usu. prominently keeled, petal epidermal cells rounded and convex; (anther with appendages), (endothecium 0 - Exacum); ovary ± bilocular, (placentae 4, pendulous), (style with secondary stigmas towards base, = diplostigmaty - Sebaea); (ovule straight), (endothelium + - Exacum); anticlinal walls of exotestal cells sinuous or not; x = 7, n = 9, 11, 15, etc.

8/184: Sebaea (75), Exacum (70). Africa, esp. Madagascar, Indo-Malesia, and to Australia and New Zealand (some Sebaea).

Age. The crown-group age of Exaceae may be some 40 m.y. (Y.-M. Yuan et al. 2003).

[Voyrieae [Chironieae [Potalieae [Helieae + Gentianeae]]]]: placentation parietal, (placentae bilobed).

Age. The age of this node was estimated at (65.2-)54.0, 46.8(-40.1) m.y. (Merckx et al. 2013c).

3. Voyrieae Gilg


Small, echlorophyllous mycoheterotrophic herbs, associated with glomeromycotes, (epiphytic); ?chemistry; axis may lack nodes but bear roots and shoots; roots and shoots both exogenous or both endogenous; (vascular bundles separate); stomata anomocytic/0; (leaves not connate basally), colleters +/0; (A extrorse); pollen variously clumped, (asymmetric), 1-6-porate, exine smooth to scabrate, orbicules 0; placentae strongly bilobed, stigma expanded, capitate to infundibular; (ovules straight, no integument, or anatropous, one integument, endothelium +, nucellar cap +; C marcescent or not; seeds dust-like, embedded in the swollen placenta or not; exotesta +; endosperm cellular or initially nuclear, present to almost absent, embryo undifferentiated to minute, 4-celled; n = 16-20.

1/19. Tropical America, Voyria primuloides in Africa (map: from Maas & Ruyters 1986; Raynal-Roques 1967).

[Chironieae [Potalieae [Helieae + Gentianeae]]]: xanthones, L-(+)-bornesitol +; (interxylary phloem +).

4. Chironieae Endlicher

(Shrubs); distinctive 6-substituted xanthones; extrafloral nectaries complex, aggregated; flowers (2-)4-5(-12)-merous, monosymmetric by androecium or not; K connate; (pollen in tetrads); n = 10, 13-15, 17, etc.

26/160: Centaurium (50). Tropics and warm N. temperate.

Synonymy: Chironiaceae Berchtold & J. Presl, Coutoubeaceae Martynov

[Potalieae [Helieae + Gentianeae]]: nectary +.

Age. This node is about 64-37.7 m.y.o. (Favre et al. 2016, q.v. for other estimates).

5. Potalieae Reichenbach

Large trees to lianes or herbs, (prickly); C-glucoflavones +; nodes 5 or more:5 or more; epidermal and cortical sclereids + [?all]; (massive sheathing stipule-like structure); flowers 3-16(-24)-merous; K basally connate; (anthers versatile), (filaments basally connate); pollen often porate; syncarpy congenital [?all]; (fruit a berry); n = ?

14-18/163: Fagraea (75), Lisianthus (30). Pantropical.

Age. Crown-group Potalieae are 40.3-33.7 m.y.o. (Favre et al. 2016).

Synonymy: Potaliaceae Martius

[Helieae + Gentianeae]: ?

Age. This node is dated to 60.7-32.2 m.y.a., older than other estimates (Favre et al. 2016).

6. Helieae Gilg

(Shrubs); vessels often in multiples; extrafloral nectaries simple; (inter/intrapetiolar sheaths, stipules +); flowers (4-)5(-6)-merous, monosymmetric by androecial arrangement or not; K lobes with abaxial glandular areas; C in bud pointed (rounded); (corona at adaxial base of A); pollen in tetrads, polyads (monads), exine elaborate; G with basal glandular areas, style often long, stigmas bilamellate, twisted and flattened when dry; (C persistent in fruit); n = ?

23/218: Macrocarpaea (110), Symbolanthus (30). Tropical Central and South America, Caribbean.

Age. Crown-group Helieae are 30-13.3 m.y.o., quite similar to other estimates (Favre et al. 2016).

7. Gentianeae Colla

Distinctive xanthones, C-glucoflavones +, (fructans/inulin +); (K 0 - Obolaria); C with fringe of hairs, vascularized or not, or scales, (folds between C lobes), (one or two nectaries on C - Swertia et al.), (nectaries naked or variously enclosed); tapetal cellls uni-(bi)nucleate; pollen striate (echinate); (nectaries naked at the base of G - Gentianinae), style often short or 0, (hollow); (ovules straight, hemitropous, etc.), integument 2-20 cells across; (antipodal cells multinucleate - e.g. Halenia, polyploid - e.g. Swertia); seeds larger; embryo small; n = >5, very variable.

18/975: Gentiana (360), Gentianella (250: polyphyletic), Swertia (168: ?polyphyletic), Halenia (80). North temperate, esp. eastern Asia, to New Guinea (some Tripterospermum) and Africa and Madagascar (some Swertia).

Age. Crown-group Gentianeae are 52.8-29.7 m.y.o., somewhat older than other estimates (Favre et al. 2016).

Synonymy: Obolariaceae Martynov

Evolution: Divergence & Distribution. Merckx et al. (2013c) and Matuszak et al. (2015) give other dates, etc., for the family.

Since Voyria primuloides, the only African species of the otherwise neotropical genus, diverged from the others somewhere between 28-12 m.y.a., LDD across the Atlantic is probably responsible for its disjunction (Merckx et al. 2013c). Von Hagen and Kadereit (2001) suggested that Gentianella moved into South America from the north and diversified considerably in the Andean region; there are ca 170 species in South America, of which ca 48 are restricted to the páramo (Sklenár et al. 2011), versus 42 in the whole of the northern hemisphere. From the Andes it moved on to New Zealand by long distance dispersal. There was an increase in diversification of Halenia only after it moved into Central and South America within the last 1 m.y., not when it first acquired corolla spurs; there were three separate colonizations of South America. The genus may originally have been from Central or East Asia, and its stem group age is ca 11.8 m.y. (von Hagen & Kadereit 2003). The wide distribution of Exacum was also probably attained by dispersal (Y.-M. Yuan et al. 2005). For diversification and "key innovations" in the small (south)east Asian and largely alpine clade of subtropical taxa sister to the speciose Gentiana, see Matuszak et al. (2016), while Favre et al. (2016) suggested that Gentiana itself has been on the Qinghai-Tibet plateau region for the last ca 34 m.y., whence it dispersed to montane regions in much of the rest of the World, indeed, the Qinghai-Tibet plateau region has been very important for the evolution of Gentianeae as a whole.

Ecology & Physiology. Mycoheterotrophic taxa have evolved in the three basal clades in the family (Bidartondo et al. 2002; Merckx et al. 2013c). Both autotrophic and mycoheterotrophic species are found in genera like Exochaenium and Exacum; some species of Exochaenium may even be parasites (Kissling 2012). Voyria in Panamanian forests is sensitive to the amount of phosphorus in the soil, disappearing when it increased above 2 mg P kg-1 (Sheldrake et al. 2017) - possibly a general phenomenon for mycoheterotrophs associated with glomeromycotes. For mycoheterotrophism in general, see Hynson et al. (2013).

Root hairs are generally absent in Voyria, but they are present in V. primuloides and also in V. aphylla where its roots abut those of other plants and also litter; fungal penetration occurs in the former situation (Imhof 1999a). The roots of these other plants are described as being decomposed at the point of fungal attachment, although apparently only locally, and carbon exchange may occur via the fungi (Imhoff 1999a), so perhaps parasitism occurs?

Pollination Biology. Swertia and other Gentianeae sometimes have fimbriate appendages and nectaries on the petals. Halenia has flowers with five nectar spurs, uncommon in angiosperms (von Hagen & Kadereit 2003). Most species of Sebaea s. str. have a pair of collateral secondary stigmas at the base of the style (Kissling et al. 2009b), apparently unique in the angiosperms.

Pollination of the mycoheterotrophic Voyria is mostly by bees. The pollen is often clumped, the clumps being held together by the tubes of pollen grains that have already germinated and/or by secretions from the anthers; the anthers are borne close together around the style or stigma (Hentrich 2008; Hentrich et al. 2010a).

Bacterial/Fungal Associations. Paris-type endomycorrhizae involving Glomeromycota are common in Gentianaceae, including the mycoheterotrophic members (Imhoff 1999, 2009; Franke et al. 2006). The Glomus involved in mycoheterotrophic relationships in Voyria and Voyriella are quite close and also to Glomus in other mycoheterotrophic vascular plants (Winther & Friedman 2008). For details of the association, see Imhof et al. (2013).

Chemistry, Morphology, etc. Gentianaceae plants are often bitter-tasting because of the iridoids they contain, while Exacum may be foetid. Flavone-O-glycosides are known from two species of Exacum, alone in the family. The wood of Helieae shows paedomorphic characteristics (Carlquist & Grant 2005). 1:3 nodes are scattered through the family, e.g. Exacum, Gentiana and Sabatia. Although Gentianaceae are not supposed to have stipules, Potaliinae in particular, and especially Fagraea, have inter/intrapetiolar sheaths and auriculate structures at the nodes; for the diversity of stipule-like structures in Macrocarpaea (Helieae), see Grant and Weaver (2003). There are different kinds of extrafloral nectaries in the family, and the survey begun by Dalvi et al. (2013) could usefully be extended.

Corolla tube formation for some taxa has been described as being late-early. Exacum has an imbricate corolla (and calyx), and the flower is monosymmetric because of the orientation of the androecium and style and curvature of the pedicel (Ronse de Craene 2010). There are sometimes two almost stamen-like appendages on either side of the ovary of Voyria, perhaps modified nectaries, indeed, I have not done justice to the variation in nectaries in the family, and, as Pringle (2014: p. 6) noted, "the flowers of most species produce nectar". In one major clade of Sebaea secondary stigmas develop towards the base of the style; this is associated with the postgenital fusion of flat carpels (Kissling et al. 2009b). Gentiana has ovules over almost the entire inner surface of the loculus. An endothelium is sometimes reported from Gentianaceae (Kapil & Tiwari 1978), however, as Shamrov (1996) describes this, it consists of one or two layers of cells of the integument that are elongated periclinally, not more or less anticlinally enlarged, as is common. The multiplicative integument of Orphium frutescens it is about 6 cells across at anthesis (Hakki 1999). The considerable variation in integument thickness in the family needs to be put into a phylogenetic context.

Cotylanthera (= Exacum) has straight, ategmic ovules, as have some Voyria. The polarity of the embryo sac in such cases is reported to have been inverted 180o, the egg cell being near the chalaza (Bouman et al. 2002; see also Suessenguth 1927). However, it is perhaps more likely that the ovule is anatropous, but the ovules are so highly reduced that few landmarks are left to be able to tell; the funicles may also lack vascular tissue (Bouman et al. 2002). The embryos of some of mycoheterotrophic taxa have very reduced cotyledons. From illustrations in Johow (1895) there appear to be two parietal cells in Voyria, and although he emphasized that the embryo sac developed from the uppermost (micropylar) megaspore, he illustrated the lowermost cell in that role.

Potalieae-Potaliinae are timber trees (secondarily woody?) with multilacunar nodes and cortical sclereids; the flowers of Anthocleista and Potalia are up to 16-merous (for further discussion, see euasterids), the corolla is deciduous, the pollen porate, carpellary fusion is congenital, and the fruits are berries. Young plants of Anthocleista have leaves over 2 m long. The group is palynologically heterogeneous (Nilsson et al. 2002).

For additional information about Gentianaceae, see Wood and Weaver (1982), Struwe and Albert (2002), Struwe et al. (2002), Merckx et al. (2013a: mycoheterotrophic taxa), Pringle (2014), Struwe (2014), Ho and Liu (2015: Swertia, etc.) and the Gentian Research Network, all general, for chemistry, see Jensen and Schripsema (2002); for nodal anatomy, see Post (1958); for general embryology, see Maheswari Devi (1963) and Hakki (1997); for ovule development, etc., see Stolt (1921: integument thickness varies within Gentiana; postament or basal projection of embryo sac), Shamrov (1996), Bouman and Schrier (1979), Vijayaraghavan and Padmanaban (1968), Akhalkatsi and Wagner (1997), Xue et al. (2007) and Li et al. (2015); for orbicules, see Vinckier and Smets (2000a); for pollen, see Nilsson (2002), Nilsson et al. (2002) and Chassot and von Hagen (2008: Swertia); and for the gynoecium, see Shamrov and Gevorkyan (2010b).

For more information on the morphology, etc., of mycoheterotrophic taxa, see Oehler (1927); for information on Voyria in particular, see Johow (1885, 1889: anatomy, seed, etc.), Maas and Ruyters (1986), Bouman and Devente (1986), and Bouman and Louis (1990), seeds, and Franke 2002 (Voyria flavescens).

We need more basic anatomical, chemical and developmental information about Saccifolieae, Exaceae and Voyrieae if the evolution of Gentianaceae is to be understood.

Phylogeny. Relationships between some of the tribes are still not well supported (Molina & Struwe 2009; Merckx et al. 2013c; Struwe 2014), in particular, the position of Voyria remains somewhat uncertain - it may have diverged before Exaceae, not after it, as suggested above. Indeed, although there is evidence from pollen, etc., that Voyria is not particularly similar to the mycoheterotrophic Voyriella, etc., its immediate relationships are unclear, although it has bicollateral vascular bundles like many other Gentianales in this part of the tree. See Albert and Struwe (1997) for a morphological phylogenetic analysis of Voyria - there is much useful morphological information. {Saccifolieae [Exaceae [Chironieae [Gentianeae + Helieae + Potalieae]]]] is probably the best way to summarize other relationships in the family (e.g. Struwe 2014; L.-L. Yang et al. 2016). Z.-D. Chen et al. (2016) do not recover quite the same basal relationships in Chinese Gentianaceae, but the vast majority of species they examined are in Gentianeae.

The Guayanan Saccifolium, with its distinctive ascidiate leaves, was originally placed in a family by itself, but it is in a clade with the mycoheterotrophic Curtia, Voyriella, etc., that is sister to all other Gentianaceae (e.g. Thiv et al. 1999; Struwe et al. 2002; see also Refulio-Rodriguez & Olmstead 2014, c.f. Struwe et al. 1998); the glandular bodies in the leaf axils of Saccifolium are best interpreted as colleters.

For the phylogeny of Exaceae, see Y.-M. Yuan et al. (2003) and Kissling et al. (2009a: Sebaea s.l. is paraphyletic), and within Sebaea s. str., there are two major clades; in the one that has secondary stigmas, S. pusilla, sister to the rest of the clade, lacks these stigmas (Kissling et al. 2009b). Mansion (2014; see also Mansion & Struwe 2004) clarified relationships within Chironieae-Chironiinae, many of which are moderately to well supported. For relationships in Helieae, morphologically variable and all Neotropical, see Struwe et al. (2009) and especially Calió et al. (2016). Relationships within Fagraea (Potalieae) have recently been clarified, and the variation in tree architecture there makes more sense (Wong & Sugumaran 2012). Within Gentianeae, Gentianella seems to be polyphyletic (von Hagen & Kadereit 2001), while Swertia, too, may be polyphyletic (Chassot et al. 2001; Kadereit & von Hagen 2003), indeed, relationships in the general Swertia/Halenia area are poorly understood (H.-C. Xi et al. (2014). Relationships within Gentianineae are being clarified, with the recently-described Metagentiana probably being polyphyletic (Chen et al. 2005b; Favre et al. 2010, 2014; Matuszak et al. 2016).

Emblingia has been placed here (Savolainen et al. 2000a), but a position in Brassicales in its own family (q.v.) is justified on both molecular and morphological grounds.

Classification. For an infra-familial classification of Gentianaceae, see Struwe et al. (2002) and especially Struwe (2014), also the Gentian Research Network.

For discussion over generic limits in Helieae, very problematic for a long time, see Calió et al. (2016). Kissling et al. (2009a) and Kissling (2010) have divided the polyphyletic Sebaea into three genera. Ho and Liu (2015: p. 21) suggested that "all infrageneric categories [of Swertia] ... might be created as independent genera if they were shown to be monophyletic units", but in the absence of a phylogeny, it is unclear if this will be necessary. There are suggestions that the monophyletic Fagraea should be dismembered (Wong 2012 and references) and members of a small clade of subtropical gentians sister to Gentiana s. str. have been placed in five genera (Favre et al. 2014); both seem a little excessive.

Previous Relationships. Anthocleista, Fagraea and Potalia used to be in Loganiaceae (Struwe & Albert 2000), but details of their iridoid chemistry are very gentianaceous and they are well embedded in the family (e.g. Backlund et al. 2000).

APOCYNACEAE Jussieu, nom. cons. - hierarchy below below very much under construction -   Back to Gentianales


Lianes, climbing by twining, to evergreen trees (herbs); tryptophane-derived, steroidal [pseudoalkaloids, pregnane skeleton], indolizidine alkaloids, route II decarboxylated iridoids +, (tanniniferous); (cork cambium deep-seated - Rhazya); pericyclic fibres 0 [always?]; (vessel elements with scalariform perforation plates), vessels single or in radial groups; tracheids in ground tissue; laticifers +, not articulated (articulated), latex white; (petioles also with adaxial bundles); stomata usu. paracytic (anomocytic, actinocytic); leaves (spiral), lamina vernation usu. flat or conduplicate, ("stipules" +, cauline); K with basal adaxial colleters, C left-contorted, postgenital connation forming the upper tube [above the insertion of the A], (corona from C); anthers ± connivent, entirely fertile, not lignified, filament short; secondary pollen presentation +, pollen transported in foam; pollen surface usu. smooth, ± perforate, intine in interapertural areas 3-layered, (in apertural areas thin); nectary as separate lobes, receptacular, or gynoecial, or 0; G apocarpous, (-8), (collateral), styluli elongated, apices alone postgenitally syncarpous, stylar head swollen, uniformly receptive, not differentiated, adherent to A, wet or dry; ovules (hemitropous), integument 6-9 cells across; seeds flattened (rounded); exotestal cells with all walls thickened, (flattened mesotestal crystalliferous cells); (chalazal endosperm haustorium +); extensive polyploidy including triploids, protein crystalloids in the nuclei; also sporophytic incompatibility system present.

400[list]/4,555: 5 subfamilies and 25 tribes below; of the subfamilies, the first two in particular are wildly paraphyletic. Largely tropical to warm temperate (map: from Hultén 1968; see also maps below). [Photo - Flower, Fruit.]

Age. Rapini et al. (2007) calibrated the age of crown-group Apocynaceae at ca 54 m.y., but Bell et al. (2010) suggested an age of only ca 21 m. years.

1. "Rauvolfioideae" Kosteletzky - this includes the next 11 tribes, 1A-1K.

1A. Aspidospermateae Miers

Trees or shrubs; (leaves spiral); calycine colleters 0; (C right-contorted); (stylar head with basal collar - Haplophyton); fruit a drupe or follicle, seeds winged, (with micropylar and chalazal coma - Haplophyton).


[Alstonieae [[Vinceae [Willughbeieae + Tabernaemontaneae]] [Melodineae, Hunterieae, Amsonieae, Alyxieae, Diplorhynchus [Plumerieae [Carisseae + APSA clade]]]]]: apical appendages of stigmatic head not secretory.

Age. The age for this node is (82.8-)63.2(-45) m.y. (Tank & Olmstead 2017).

1B. Alstonieae G. Don

Trees or shrubs; calycine colleters 0/+; (C right-contorted); ?anthers; (stylar head differentiated); fruit a follicle; seeds with coma at both ends, winged, or hairy.

2/47: Alstonia (45). Africa, Southeast Asia, Malesia to the Pacific.

[[Vinceae [Willughbeieae + Tabernaemontaneae]] [Melodineae, Hunterieae, Amsonieae, Alyxieae, Diplorhynchus [Plumerieae [Carisseae + APSA clade]]]]: ?

1C. Vinceae D. Don.

Trees, shrubs (lianes, herbs); calycine colleters 0; (C right contorted); anthers free from stigma, (with apical appendage); (only one G develops), stylar head differentiated, apical unlobed wreath of hairs, basal collar; fruit a drupe, moniliform with several drupelets, or follicle; seeds (1-2), (warty, hairy or winged); (endosperm 0 - Kopsia).

9/153: Rauvolfia (60), Ochrosia (40). Pantropical, esp. Old Word (temperate - Vinca).

Synonymy: Ophioxylaceae Martius, Vincaceae Vest

[Willughbeieae + Tabernaemontaneae]: G [2] [could be placed here].

1D. Willughbeieae A. de Candolle

Lianes, branches with terminal tendrils, trees, or shrubs (rhizomatous); calycine colleters +/0; G [2], placentation axile to parietal; fruit a berry, (seed 1).

18/130: Landolphia (60).

Synonymy: Pacouriaceae Martynov, Willughbieaceae J. Agardh

1E. Tabernaemontaneae G. Don

Shrubs or trees (lianas); calycine colleters several to many, basal; A sessile, not cohereing to stigmatic head (cohering), anthers with thick, lignified guide rails; nectaries paired, (0); G [2], placentation axile to parietal, or apocarpous, apes of stylar head bilobed, with a five-lobed upper crest and a thickened basal flange (not); fruit a berry/berrylet, or follicular [Tabernaemontaninae], (K persistent); seed with aril, ± ruminate, with deep hilar groove.

15/150: Tabernaemontana (110). Northern South America (Ambelaniinae) and pantropical (Tabernaemontaninae).

[Melodineae, Hunterieae, Amsonieae, Alyxieae, Diplorhynchus [Plumerieae [Carisseae + APSA clade]]]: ?

1F. Melodineae G. Don

Trees, or shrubs; calycine colleters usu. 0; G [2], placentation axile, or apocarpous; fruit a berry, or follicle; seeds winged.

5/. Melodinus (75).

1G. Hunterieae Miers

Shrub or small trees (lianas); anthers?; calycine colleters usu. +; G 2-5; fruit berrylets.


1H. Amsonieae M. E. Endress

Small shrubs to perennial herbs; leaves spiral; calycine colleters 0; stylar head differentiated, with basal collar; fruit a follicle; seeds not flattened.


1I. Alyxieae G. Don

Shrubs, trees or lianes; indole alkaloids 0; (leaves spiral); calycine colleters 0; anthers completely fertile; pollen grains 2-3-porate, barrel- or irregularly-shaped, ectoapertures with thickened margins, (inaperturate, in tetrads - Condylocarpon); G also [3-5], stylar head with apical appendages also secretory; fruit a berry or drupe, moniliform with several drupes, or follicular; seed with aril, ± ruminate, with deep hilar groove, or winged at both ends, (ruminate); n = 9.

7/. Alyxia (120). (northern Brazil and Guyana).

[Plumerieae [Carisseae + APSA clade]]: ?

1J. Plumerieae E. Meyer

Shrubs, trees (lianes); iridoids, cardenolides [cardiac glycosides] +; leaves spiral (opposite); calycine colleters 0/+; (corona +); anther (sagittate, adnate to style head), (apex sterile, plumed); (G [2] - postgenitally), placentation parietal, stylar head differentiated; 2 ovules/carpel; fruit a drupe or samaroid, or follicle; seeds winged.


Synonymy: Cerberaceae Martynov, Plumeriaceae Horaninow

[Carisseae + APSA clade]: ?

1K. Carisseae Dumortier

Shrubs to trees; indole alkaloids 0, (cardenolides [cardiac glycosides] +); (branched thorns +); calycine colleters usu. 0; (C right-contorted); A well above stylar head; G [2], placentation parietal to axile, or apocarpous; fruit a berry.

2/12. Old World tropics.

Synonymy: Carissaceae Bertolini

[Wrightieae [Nerieae [Maloutieae [[Periplocoideae [Echiteae, Mesechiteae, Odontadenieae]] [[Rhabdadenieae + Apocyneae] [Baisseeae [Secamonoideae + Asclepiadoideae]]]]]]] / APSA clade (Apocynoideae, Periplocoideae, Secamonoideae, Asclepiadoideae): iridoids 0 [this level?], (cardenolides + [cardiac glycosides]), homospermidine synthase gene +; anthers with sagittate lignified basal appendages [guide rails]; pollen porate; anthers firmly adnate to style head [forming gynostegium], retinaculum formed by trichomes [region of stamen by which it attaches to style head]; stylar head differentiated both radially and vertically, with a thickened basal flange, receptive basally; fruit a follicle; micropylar coma +. Where?: A inserted well below bases of corolla lobes; n = (6-) 11 (12).

Wrightieae G. Don

C left- or right-contorted; corona +/-; ([G 2]); chalazal coma + (and micropylar, deciduous).

3/29: Wrightia (23). Old World tropics.

[Nerieae [Maloutieae [[Periplocoideae [Echiteae, Mesechiteae, Odontadenieae]] [[Rhabdadenieae + Apocyneae] [Baisseeae [Secamonoideae + Asclepiadoideae]]]]]]: C right-contorted; exine infratectum granulate [?all].

Nerieae Baillon

(Succulent) shrubs or trees, (lianas); (pyrrolizidine alkaloids + - Alafia); (leaves spiral); (corona +); anthers with long apical appendage; G free to connate; coma also chalazal.

6/47: Strophanthus (38). Africa (most) and Europe to Japan and Malesia.

[Maloutieae [[Periplocoideae [Echiteae, Mesechiteae, Odontadenieae]] [[Rhabdadenieae + Apocyneae] [Baisseeae [Secamonoideae + Asclepiadoideae]]]]]: ?

Malouetieae Müller Argovensis

Plant cactus-like, with spines; leaves spiral; calycine colleters 0; anthers weakly attached to stylar head; G free, stylar head with five basal projections; chalazal coma +.


[[Periplocoideae [Echiteae, Mesechiteae, Odontadenieae]] [[Rhabdadenieae + Apocyneae] [Baisseeae [Secamonoideae + Asclepiadoideae]]]]: plant vine/liane; few wide vessels and several narrow vessels in clusters; vasicentric tracheids +; fibres [not tracheids] in ground tissue; nectaries 5, (basally connate), surrounding base of ovary [?level].

[Periplocoideae [Echiteae, Mesechiteae, Odontadenieae]]: ?

Periplocoideae Endlicher


Shrubs or slender climbers, (roots tuberous); flowers to 10 mm long (to ca 9 cm -Cryptostegia); C (valvate), tube formation intermediate, corona corolline, morphology various; stamen-corolla tube very short, staminal feet erect, connate, forming tube around ovary; nectar secreted on margins of staminal feet [alternistaminal], receptacular nectary 0; anthers without lignified guide rails; tapetal cells uni(bi)nucleate; pollen in tetrads, inner and outer walls differentiated, grains 4-16 porate; pollen collected on spoon-like structure, basal sticky viscidium [translator]; retinaculum formed by cellular fusion; exotestal cells unthickened [Periploca]; embryo color?.

31/180. Old World, esp. Africa, tropics to dry temperate (map: Good 1952).

Age. The crown-group age of Periplocoideae is estimated to be (40-31.5(-23.4) m.y. (Joubert et al. 2016).

Synonymy: Periplocaceae Schlechter, nom. cons.

[Echiteae, Mesechiteae, Odontadenieae] / New World clade: (pyrrolizidine alkaloids +).

Echiteae Bartling

Woody lianes (small trees; herbs); (latex translucent); calycine colleters +, position variable; (C valvate), (corona +); guide rails narrow, (filaments spirally twisted - some Parsonsia); stylar head fusiform, basal collar narrow; (n = 6).

19/ Parsonsia (120), Prestonia (65). New World, tropical, also New Caledonia (two genera) to Australasia and South East Asia (Echites).

Mesechiteae Miers

Colleters on adaxial surface of leaf.

5/ Mandevilla (115), Forsteronia (50). New World.

Odontadenieae Miers

7/ New World.

[Rhabdadenieae + Apocyneae] [Baisseeae [Secamonoideae + Asclepiadoideae]]: microsporogenesis successive (simultaneous), grains in tetrads, inaperturate or variously porate.

[Rhabdadenieae + Apocyneae]: ?

Rhabdadenieae M. E. Endress

Slender lianas to perennial herbs; wood fibres very thin-walled, parenchymatous; calycine colleters 0; guide rails truncate, fused to filament; stylar head cylindrical, apically hairy, basal collar +.

1/4. Tropical America.

Stamen-corolla tube very short; stylar head fusiform (with strap-like bands of adhesive), no basal collar. [goes where?]

Apocyneae Reichenbach / Old World clade

Shrubs, lianes, or herbs; (pyrrolizidine alkaloids + - Anodendron); (leaves spiral); calycine colleters +; (C left-contorted); stylar head usu. broadest at the middle, basal collar 0 (+).

24/. Largely Malesian-South East Asian, also North Temperate (Apocynum).

[Baisseeae [Secamonoideae + Asclepiadoideae]]: colleters on adaxial surface of leaf; stamen-corolla tube very short; G initially half inferior, stylar head without basal flange.

Baisseeae M. Endress

Large lianes; (trichomes branched); (leaves with domatia), (colleters axillary - Dewevrella; (filaments long, spirally twisted first in one direction and then the other - Dewevrella); (stylar head with strap-like bands of adhesive).

4/32: Baissea (20). Old World Tropics, esp. Africa.

[Secamonoideae + Asclepiadoideae]: lianes common; (fructans/inulin +), monoterpene indole alkaloids 0; C tube formation intermediate; A inserted well below bases of corolla lobes, corona usually staminal [common vascular supply with A, filaments 0, anthers inserted on top of fused tube/specialized ring corona/staminal feet], nectary staminal, [produced in alternistaminal sections of tube behind guide rails formed by wings of adjacent anthers]; endothecium not fibrous; pollinia of the one pollinarium from half anthers of adjacent stamens, erect, lacking outer walls, retinaculum formed by cellular fusion, caudicles/translator arms short, with hardenened apical corpusculum [adhesive]; pollen tetrads with outer and inner walls differentiated [inner walls have intine bridges] [?level], orbicules 0; endosperm nuclear (cellular), embryo chlorophyllous.

Age. This node was dated to ca 42 m.y. (Rapini et al. 2007).

Secamonoideae Endlicher

Lianes, climbing by twining; (colleters on adxaial surface of leaf); K with a single trace), (C left-contorted); pollinia 4; granular layer thick.

8/170: Secamone (100). Old World, esp. Madagascar, tropics to temperate.

Asclepiadoideae Burnett


(Interxylary phloem +); colleters on adaxial surface of leaf blade; C with corona, also connate corona on staminate and interstaminate regions; anthers bisporangiate, dithecal, pollinia 2; tapetal cells uninucleate; pollen with granular layer of exine thin; nectar usually accessible at or near base of guide rails; (pollen receptive areas areas 5, on the anther wings at the top of the guide rails), (compitum 0); mitochondrial PEP subunit β" rpoC2 pseudogene [from chloroplast]; n = (9-14).

214/2365. Tropics to temperate, drier areas esp. in Africa (map: see Good 1952). [Photo - Flower, Flower, Flower, Fruit.]

Age. Crown group Asclepiadoideae were estimated to be ca 37 m.y.o. (Rapini et al. 2007).

A. Fockeeae H. Kunze, Meve & Liede

Plants with massive tuberous roots; connective appendages +, inflated; (anther secretes sporopollenin wall around pollinium, pollen appear to be in monads when mature - Cibirhiza).

2/9. Drier parts of southern and eastern Africa, Arabia.

[[Eustegieae + Asclepiadeae] [Marsdenieae + Ceropegieae]]: (often epiphytic); (phenathroindolizidine alkaloids); (leaves spiral); anther secretes sporopollenin wall around pollinium, pollinia with translator arms [caudicles], (orbicules + - Riocreuxia); outer and inner walls of tetrads not differentiated, pollen appear to be monads when mature.

[Eustegieae + Asclepiadeae]: mitochondrial rpll pseudogene [from the plastid].

B. Eustegieae Liede & Meve

Latex clear; leaves (spiral), lamina palmately lobed, (margin with a few teeth).

2/6. The Cape, southeast Africa.

C. Asclepiadeae Duby

(Erect, non-twining herbs and shrubs); (rootstocks thickened), (stem succulents - Cynanchum); pollinaria horizontal or pendent; (n = 9).

87/. Cynanchum (330), Matelea (180), Asclepias (100), Gonolobus (100), Oxypetalum (90), Ditassa (75), Tylophora (50).

Synonymy: Asclepiadaceae Borkhausen, nom. cons., Cynanchaceae G. Meyer

[Marsdenieae + Ceropegieae]: ?

D. Marsdenieae Bentham

(Plants shrubby); (latex clear); (pollinia with pellucid margin along proximal side); (exotestal cells with outer walls unthickened - Hoya).

26/. Hoya (90[-200+]), Marsdenia (100), Dischidia (80),

E. Ceropegieae Orban

Plants commonly ± erect; (stem succulents - esp. stapeliads), (root tubers +); latex clear; C valvate; pollinia with pellucid margin along distal side; (hypocotyl massive, cotyledons very small).

47/. Ceropegia (160), Brachystelma (100), Stapelia (70), Orbea (55), Huernia (50), Heterostemma (48), Caralluma (47).

Synonymy: Stapeliaceae Horaninow

Evolution: Divergence & Distribution. For dates of divergences within the family, etc., see Rapini et al. (2007) and Liede-Schumann et al. (2012).

Endress (2011a) thought that a key innovation within Gentianales was the possession of pollinaria, presumably to be optimized at the [Secamonoideae + Asclepiadoideae] node. Pollen morphology and development is very variable in Apocynaceae, and the optimization of such characters above is only tentative. Pollinia may have increased pollination efficiency by generalist pollinators in the rather small populations growing in the rather dry areas many members of the family prefer - a reduction of the Allee effect. Asclepiadoideae, often herbs, are derived members of this clade (Livschultz et al. 2011), and they are diverse and highly endemic in southern Africa in particular (Ollerton et al. 2003), about 700 species having been recorded from there (Johnson 2010). Diversification of Ceropegieae, with some 670 species, occurred around 3 m.y.a. as Africa became more arid (Bruyns et al. 2015: estimate younger than in Rapini et al. 2007). Meve and Liede (2002b) discuss a number of apparently quite recent Africa→Madagascar movements in Asclepiadoideae, with the odd movement in the opposite direction. For diversification in Periplocoideae, see Joubert et al. (2016); Phyllanthera grayii, from northeast Australia (other species up to South East Asia), and Petopentia, from South Africa, are successively sister to the rest of the subfamily.

Within "Apocynoideae" genera in major clades usually are from either the Old or the New World, with little overlap between the two (Livschultz et al. 2007). There is also substantial geographical structuring of clades within groups like e.g. Asclepiadoideae (Goyder 2006 for a summary); basal clades of the large genus Cynanchum are African (Khanum et al. 2016).

All tribes in "Rauwolfioideae" can be more or less readily distinguished by a combination of features in their wood anatomy (Lens et al. 2008b), but such characters remain to be integrated into the phylogeny.

Ecology & Physiology. Members of the old Asclepiadaceae are the most speciose scandent group in tropical New World forests, those of the old Apocynaceae somewhat less so, and all told ca 1,350 species are involved, although some of these are quite small plants; in Africa Apocynaceae are perhaps the most prominent group of scandent species (Gentry 1991). Livschultz et al. (2011) proposed that [Asclepiadoideae + Secamonoideae] moved into drier habitats, the large rainforest lianes of Baisseeae representing the ancestral habit/habitat of the whole milkweed clade. More or less erect growth forms have evolved from lianes in Secamonoideae (Lahaye et al. 2005). The Hoya-Dischidia clade includes a large number of epiphytic climbers, unfortunately, details of the evolution of this distinctive habitat preference/habit are unclear (Wanntorp et al. 2014).

Succulence is widespread in the family, particularly in Periplocoideae (root succulents) and Asclepiadoideae-Ceropegieae (especially stem succulents). Nyffeler and Eggli (2010b) estimate that there are 74 genera containing 1151 species of succulents; 65 of these genera, mostly small, include only succulent taxa (Meve & Liede-Schumann 2010). There are about 400 species of stem succulent Ceropegieae in the Old World alone, with centres of distribution in Arabia, East Africa and southern Africa (Meve et al. 2004). Stapeliads, ca 340 of these species, seem to have evolved in the northern hemisphere, then moved into southern Africa, and then fanned out throug the drier parts of the continent, Madagascar and Arabia (Bruyns et al. 2014a) - and this all in the last eight million years or so (Rapini et al. 2007). The embryo in a number of these succulent taxa has a massive hypocotyl and very small cotyledons, and the leaves in the adult plant may be reduced to minute projections (Bruyns 2005).

Pollination Biology and Seed Dispersal. In all Apocynaceae, the anthers are closely associated with a swollen stigmatic head (e.g. Nilsson et al. 1993). In genera like Alyxia all or most (not the very apical) cells of the stigmatic head secrete a sticky polysaccharide-terpenoid material to which the pollen adheres - basically, secondary pollen presentation; there are no localized receptive and secretory areas on the stigma. Such taxa predominate in the basal grade of "Rauvolfioideae". Such stigmas are considered here to be the basic condition for the family, but they are perhaps derived, and more than once, the differentiated stigma described below being plesiomorphic for the whole family (Simõs et al. 2007a; see especially Schick 1980, 1982, also Shamrov & Gevorkyan 2010a and Morokawa et al. 2015 for the morphology of the stigmatic head). Taxa with an otherwise undifferentiated stylar head may have a pair of apical "stigmatic lobes", although these do not function as stigmas (Albers & van der Maesen 1994). In taxa with spatial differentiation within the stigmatic head, pollen is deposited onto the apex of the swollen head; sticky material is secreted immediately below, and pollen germinates only at the base of the head (e.g. Albers & van der Maesen 1994). The gynostegium, formed by the post-genital fusion of anthers and stigma, develops when the connective tissue of the anther becomes adnate to the stigmatic head (the staminal retinacule of Simões et al. 2007b). Commonly in "Apocynoideae" pollen from thecae of adjacent anthers mixes because dehiscence is more or less latrorse, whereas pollen from the two thecae of the one anther does not mix because the intervening connective is adnate to the stigmatic head, that is, the basic spatial arrangement of the androecium is the same as that in Asclepiadoideae (see also Schick 1982). This is a very complex system, and in Tabernaemontaneae several features - an androecium with thick, lignified guide rails (these are formed from the wings of adjacent anthers), a stylar head with a five-lobed upper crest and a thickened basal flange, and paired nectaries - are all associated, all being lost together some five times on the tree (Simões et al. 2010).

The intimate association of the androecium and gynoecium to form the gynostegium that characterizes Asclepiadoideae and Secamonoideae is postgenital. Within Periplocoideae, pollinia seem to have evolved at least three times (Ionta & Judd 2007), and certainly independently of pollinia in the old Asclepiadaceae (Straub et al. 2014). The evolution of the pollinaria that characterize [Secamonoideae + Asclepiadoideae] (see Harder & Johnson 2008) can be considered separately, although variation in the pollinarium of Fockeeae, sister to all other Asclepiadoideae, somewhat confuses the issue (see Verhoeven et al. 2003). In any event, the old idea of the evolution of the pollinia of Asclepiadaceae via Periplocaceae/Periplocoideae as some sort of intermediate needs to be revised (see also Potgieter & Albert 2001; Sennblad & Bremer 2002; Ionta & Judd 2007; esp. Livschultz et al. 2007).

Nectar in many of the old Apocynaceae is secreted by nectaries at the base of the gynoecium; these vary in number and may be connate basally or free; some taxa have nectaries in the ovary wall (Morokawa et al. 2015). In Secamonoideae and Asclepiadoideae in particular nectar may be secreted in "staminal outgrowths" from the petal-like staminal feet (i.e. the corolla + filament tissue below the anther) that completely surround the gynoecium. Kunze (e.g. 1991, 1997; Kunze & Wanntorp 2008b) show that it is secreted beneath the guide rails, although it may be accessible to the pollinator only elsewhere in the flower (Fahn 1979 suggested that the stigma itself might secrete nectar in Asclepias). A variety of floral volatiles from the family has also been characterized (Jürgens et al. 2009).

Flowers throughout Apocynaceae develop a variety of petal-like appendages. These may develop from the corolla tube (Nerium, Allamanda) or from the apices of the anthers (Adenium, Nerium). Strophanthus can have appendages at the apices of the anthers or more or less bilobed appendages in the angles of the corolla lobes, while the apex of the corolla lobe narrows into a thin, dangling process that in some species is almost 30 cm long; there is no nectary. The diversity of form produced by tissues from the corolla, stamens, and staminal feet in [Secamonoideae + Asclepiadoideae] is remarkable (see Liede & Kunze 1993 for terms used). Within Asclepiadoideae, the corona develops very late and is clearly staminal, and this is consistent with the pattern of gene expression in the flower (Livshultz & Kramer 2009), although Kunze (2005b) suggests that it is an organ sui generis - which it is, from another point of view. There is much variation in the details of the gynostegium in Asclepiadoideae (e.g., see the photographs in Pilbeam 2014). Kunze and Wanntorp (2008a) discuss corona and anther skirt evolution and they puzzle over the morphologically distinctive gynostegium of the molecularly unremarkable Hoya spartioides (Kunze & Wanntorp 2008b).

For a general survey of pollination in Apocynaceae, see Ollerton & Liede (1997). Hairs on the anthers or stigmatic head, or lignified guide rails on the side of adjacent anthers, are all involved in pollen presentation and guiding the mouth parts of the pollinator to the nectar and its pollen load to the stigma so that effective pollination occurs (e.g. Fallen 1986). An annulus or flange around the middle of the head in many ex-Apocynaceae aids in the removal of the pollen from the proboscis of the pollinator, scraping it off, while the receptive stigma itself forms a ring around the base of the head. The stigmatic flange and the lignified guide rails on the anthers together form a trap-and-guide pollination mechanism. In asclepiads nectar may be physically associated with the guide rails, the proboscis of the insect being guided to the viscidium as it probes for nectar, which thus attaches the pollinia to the pollinator (e.g. Kunze 1991); insects may even become trapped as they do this (Liede 1996). In Catharanthus roseus it was found that direct cell-to-cell communication vis plasmodesmata developing in the epidermal cells was early established as the apices of the carpels fused, pollen thus potentially being able to fertilize ovules in either carpel (van der Schoot et al. 1995). However, in at least some asclepiads there is no compitum, hence in part the common occurrence of flowers with just a single carpel fertilized. The situation is yet more complex, because in some Asclepiadoideae (?and other Apocynaceae) the receptive area for the pollinia is on the anther wings at the end of the guide rail, and pollen germination occurs there and not on the stigma (Vieira & Shepherd 2002), and/or nectar is needed for germination of the pollen grains, and this is secreted by nectaries in the stigmatic chamber (Kevan et al. 1989); there are effectively five stigmas in a flowers with two carpels.

Pollination may seem to be quite a precise process in many Apocynaceae, the complex floral morphologies guiding the movements of the pollinator. However, several species of insects can effectively pollinate the one species of asclepiad, so if the flowers seem morphologically specialized they are functionally generalists (e.g. Ollerton et al. 2003, 2007: Table 1). Thus there were 41 (low end) to 185 (high end) species of visitors to flowers of five species of Asclepias in North America, 17 to 116 of these respectively being effective pollinators (Fishbein & Venable 1996)! Ollerton et al. (2003) looked at pollination of some asclepiads in South Africa, and found that flowers pollinated by specialist insects had abundant and easily accessible nectar, and were visited by many other insects, too; furthermore, such asclepiads quite often set fruit - and apparently not by selfing - in cultivation well away from their native habitats (Bruyns 2005). On the other hand, despite the apparently functionally generalized flowers with easily-accessible nectary of Pachycarpus grandiflorus, just a single species of wasp was its effective pollinator (Shuttleworth & Johnson 2009). Other asclepiads with specialised flowers also specialised - but on common, ubiquitous visitors (Ollerton et al. 2003). Fly pollination has been studied in detail in Ceropegia (Vogel 1961); it is widespread in Asclepiadoideae-Ceropegieae and some -Asclepiadeae (see e.g. the photographs in Pilbeam 2014; Bruyns 2005). See Oelschlägel et al. (2014) for various ways to attract flies - foul smell, dark colour, dangling appendages, and the like are all found in stapeliads and other groups (for osmophores, see Plachno et al. 2010; for chemical mimicry of oviposition sites, see also Jürgens et al. 2013). In one example, about 60% of the some 60 Ceropegia examined were pollinated by a single genus of flies (Ollerton et al. 2009b: see below for the phylogeny of the genus), and such plants can be thought of as being ecologically quite specialized (Ollerton et al. 2007). Spider-hunting wasps pollinate some asclepiads, and they are not put off by the bitter nectar which deters other pollinators (Johnson 2010). Meve and Liede (1994; see also Bruyns 2005) surveyed pollination in stapeliads in general; as Bruyns et al. (2014a) note, the flowers are quite frequently more or less hidden in bushes or litter, so how the very complex morphologies of the sometimes small flowers - the coronal-gynostegium area is quite often <4 mm across - relate to pollinator activities needs investigation (fungus gnats are implicated in the pollination of some small concealed flowers - see Bruyns 2000). Bruyns et al. (2015) suggested that flies of one type or another were pollinators in this group, with large flies pollinating stapeliads, and since 10 or more asclepiad species may grow together (Bruyns 2000), details of what pollinators do in terms of con- and heterospecific pollinaria transmission would be of considerable interest. Yamashiro et al. (2008) studied details of pollination of Japanese species of Vincetoxicum; tipulids, other dipterans, moths, etc., were all involved.

Wyatt and Lipow (2007) suggest that the evolution of pollinia and the secondary apocarpy in Asclepiadoideae and Apocynaceae s.l. is connected with the post-zygotic incompatibility system that characterises Apocynaceae (?all) and at least some other Gentianales. In Ceropegieae, at least, the situation is rather like that in many Orchidaceae - natural hybrids are uncommon, but it is quite easy to make successful artificial crosses between species in different "genera" (Meve et al. 2004 for references).

Fruit and seed morphology in the old Apocynaceae is quite variable, but follicular fruits with comose seeds characterise a clade that includes the old Asclepiadaceae. At least some Asclepiadoideae have no compitum, one of the reasons for the frequent occurrence of fruits in which only a single carpel has developed.

Plant-Animal Interactions. Despite the toxic metabolites so common in Apocynaceae, there are about 50 separate groups of herbivorous milkweed-eating insects (Farrell 2001 and references). Many of these sequester the toxins and have bright aposematic warning colouration and are involved in some sort of Mullerian mimicry systems. Thus brightly-colored orange and black danaine caterpillars and bright orange aphids are to be found on Asclepiadoideae in both North America and southern Africa; the longicorn Tetraopes is often orange and black, and so on. Insects that eat cardenolide-containing Apocynaceae show convergence at the amino acid level (asparagine changes to histidine in several entirely unrelated insects at position 122 of the K-ATPase β subunit) that appears to promote cardenolide resistance; normally cardenolides inhibit the sodium-potassium (Na/K) pump by binding with this subunit (Zhen et al. 2012; Dobler et al. 2012, 2015; Whiteman & Mooney 2012 for a summary). Caterpillars of Nymphalidae-Danainae-Danaini relish Apocynaceae (Ehrlich & Raven 1964; see Ackery & Vane-Wright 1984 for a comprehensive treatment; Brower et al. 2010 for a phylogeny), but they also eat other plants with latex, including several Moraceae and Carica; Danainae-Tellervini also eat Apocynaceae (Wahlberg et al. 2009; Nylin et al. 2013). The monarch butterfly is involved in this cardenolide syndrome; the cardenolides are noxious and may protect both caterpillar and adult butterfly (e.g. Malcolm 1991; see also Dobler et al. 2011). The cardenolides may not be toxic to a few species whose caterpillars do not sequester them yet nevertheless can eat the plants, but species that do sequester cardenolides have modifications to their Na/K pump that non-sequestering species lack (Petschenka & Agrawal 2015). The ability of some insects to eat cardenolide-containing plants is then a separate issue (see also Dobler et al. 2015).

Caterpillars of the two main clades of Nymphalidae-Danainae (Danaini, Ithomiini) can be found on Apocynaceae, probably their ancestral host family (Edgar 1984; Janz et al. 2006; c.f. Wahlberg et al. 2009); the danaine clade diverged from other butterfly clades ca 89 m.y.a. (Wahlberg et al. 2009). Almost all Danaini, some 160 species, are to be found on Apocynaceae (Agrawal et al. 2012; Petschenka & Agrawal 2015). Larvae of only a few species of ithomiines are found on Apocynaceae, especially on Echiteae (Edgar 1984, as Parsonsieae). In a comprehensive morphological analysis (Wilmott & Freitas 2006) these apocynaceous-eating ithomiines, which include Tellervo, the only Old World member of the group, came out at the base of the tree (unrooted); ithomiines otherwise eat mostly New World Solanaceae, q.v..

For the possible co-evolution of the longicorn cerambycid beetle Tetraopes with Asclepias, see Farrell and Mitter (1998) and Farrell (2001); species of Tetraopes tend to eat different species of Asclepias, and Phaea, which eats other Apocynaceae, is paraphyletic with respect to Tetraopes. Hosts of seed-eating bugs of Hemiptera-Lygaeidae-Lygaeinae are concentrated in the old Apocynaceae (Slater 1976). Resistance of aphids to cardenolides may have evolved rather differently from that in other herbivores eating asclepiads (Zhen et al. 2012). These aphids seem to feed preferentially on internal phloem/adaxial phloem of leaf bundles, apparently the cardenolide transport system, so acquiring food and protection at the same time (Botha et al. 1977). However, which bundles are targeted may also depend on the age of the leaf (Botha et al. 1975). Aphids on Asclepiadoideae may on occasion even induce cardenolide production (Martel & Malcolm 2004).

For a study of the different defence syndromes of Asclepias, see Agrawal & Fishbein (2006). Although the resprouting ability of Asclepias - or simply its tolerance of herbivory - may be an effective defence against specialist herbivores (Agrawal & Fishbein 2008), the situation is complex; production of a variety of phenolics also changed with herbivory, showing an overall increase as cardenolide production decreased (Agrawal et al. 2009a). Indeed, one interpretation of the initial diversification of North American Asclepias is that this was accelerated by reduced investment in defensive traits like latex and cardenolide production (Agrawal et al. 2009b). Furthermore, there is an inverse correlation between the presence of leaf surface waxes and that of indumentum, the presence of either making it more difficult for potentially noxious insects to alight, although other plant traits are also involved (Agrawal et al. 2009c). Finally, both induced and constitutive - amount and diversity - cardenolide production increases at lower latitudes (Rasmann & Agrawal 2011; Agrawal et al. 2012 for a summary), although Moles et al. (2011b) suggest that generally such protective compounds decrease at lower latitudes. Furthermore, milkweed caterpillars can be infected by protozoan parasites, and their tolerance of and resistance to particular species of parasite depends on the species of Asclepias they are eating; tolerance and resistance are conferred separately by the plant (Sternberg et al. 2012). This whole system is very complex.

1,2-dehydropyrrolizidine alkaloids are found in some Apocynaceae, and plants with these alkaloids attract practically all Danaini butterflies, mostly males, which use them as the basis of their pheromones and for defence (Boppré 2005; Brehm et al. 2007). The monarch does not use these alkaloids in pheromones, but it does sequester them for defence (Hartmann & Witte 1995). Pyrrolizidine alkaloids are sometimes expressed in the root only, where they protect against generalist root feeders, while the absence of the alkaloids in the leaves means they do not attract specialized herbivores (Livshulz et al. 2016). Pyrrolizidine alkaloids and pentacyclic triterpene saponins variously sequestered and modified are also found in the secretions of the defensive glands of some Chrysolina and Platyophora beetles (Chrysomelidae, both very speciose genera: Pasteels et al. 2001; Termonia et al. 2002; Hartmann et al. 2003). Adult ithomiine butterflies are attracted to Apocynaceae from which they take up alkaloids, and Edgar (1984) and Brehm et al. (2007) suggested that the pyrrolizidine alkaloids of Echiteae may have been originally involved in their pharmacophagous behaviour. These pyrrolizidine alkaloids are also found in Crotalaria, Heliotropaceae and Asteraceae-Asteroideae.

Myrmecophily is known from some Malesian species of Dischidia in particular and also some species of Hoya. The plants live in ant gardens along with a variety of other angiosperms and some ferns that are formed by the activity of the ants, and these gardens can be dated to (7.9-)4.9(-1.9) m.y.a. (Chomicki et al. 2017, see also Chomicki & Renner 2015 for dates). The ants (e.g. Iridiomyrmex) inhabit modified leaves that are shaped like the finger of a glove in taxa like D. rafflesiana and they bring in dead insects, etc., into the leaf cavity; the roots of the plant permeate the decaying material, and the ants feed the plant as much as protect it (e.g. Janzen 1974c). However, some species of Dischidia are effectively free loaders on this and other plant-ant associations, their roots growing in the domatia as well, while yet other species grow independently of ants. Although the seeds of Hoya are plumed and so are apparently wind dispersed, they attract ants that take them to their nests (Janzen 1974c; Weir & Kew 1986).

Bacterial/Fungal Associations. Although Paris-type mycorrhizae are found in Gentianaceae, Loganiaceae, and Rubiaceae, Arum-type endomycorrhizae, or intermediates, are common in Apocynaceae, especially in Asclepiadoideae (Imhoff 1999).

Vegetative Variation. Seedlings of genera with opposite leaves, like Hoya, may have spiral leaves; Absolmsia, previously segregated from Hoya, has spiral leaves even at the flowering stage. In taxa such as Vallesia there are cauline "stipules", apparently colleters in a stipular position; Vallesia also has spiral leaves. Mandevilla has a distinctive ring of large, radiating, almost fleshy projections immediately below the leaves, and in other taxa there may be adaxial, scale-like structures on the petiole (Thomas & Dave 1991). A variety of stipule-like structures is also found in Stapelia and relatives; in Edithcolea grandis the "stipule" is represented by a single hair (Bruyns 2000, see also 2004), while there is a variety of hairs and other structures in the stipular position in Caralluma (Bruyns et al. 2010). In Apocynaceae like Alstonia there is an adaxial excavation at the base of the petiole in which the axillary bud is enclosed; this is often encased by secretions from the colleters.

Branching in a number of taxa is complex. The apical bud may abort, or be converted into an inflorescence, and there may be a pair/whorl of very reduced leaves separated by a very short internode from a whorl of normally-developed leaves at the end of each innovation, and these reduced leaves subtend vegetative branches or inflorescences which then appear to be in an extra-axillary position (Troll & Weberling 1990). The "lateral" inflorescences of at least some stapeliads may be displaced-terminal (Bruyns 2004), and such inflorescences are also found in Apocynum, Asclepias, etc., however, Leptadenia (Asclepiadoideae) has axillary inflorescences. The literature on such inflorescences is quite extensive, although there is no recent synthesis; see e.g. Woodson (1935), Holm (1950), Nolan (1969), Liede and Weberling (1985) and Steck and Weberling (1982).

Genes & Genomes. A rpll pseudogene (this gene is mitochondrial) is found in the plastid in Asclepiadeae, etc. (Straub et al. 2013); the chloroplast PEP subunit β" rpoC2 gene is present as a mitochondrial pseudogene throughout the subfamily, with something funny also going on in Secamone.

Chemistry, Morphology, etc. For distinctive fatty acids in the seed, see Badami and Patil (1981). Agrawal et al. (2011) summarize information on cardiac glycosides in the family; they note that the steroidal alkaloids found in Apocynaceae are strictly speaking pseudoalkaloids, since the nitrogen does not come from amino acids.

The cambium is occasionally storied. The leaves of Asclepiadoideae and many genera more basal to them have flat vernation (Cullen 1978). Cymose inflorescences of some sort are the norm in the family, and some Marsdenieae in particular have very long-lived but contracted inflorescences in which single flowers or whorls of flowers open at intervals over a year or more (Meve et al. 2009).

Endress (2016: comparison with Orchidaceae) emphasized the development of synorganization/complexity in the flowers here; synorganization lays the foundation for the development of novel structures, however, the corona, one of the most conspicuous of novel structures in Apocynaceae, is not directly the product of synorganization. There is variation in the direction of contortion of the corolla lobes (e.g. Eichler 1874). How the corolla tube is initiated in Periplocoideae is unknown. Much has been written about the homology of the various petaloid floral structures; deciding which structures on different flowers are directly comparable (see Remane's criteria) can indeed be very difficult. If the staminal feet in Periplocoideae are considered similar to the fused basal tube of [Secamonoidae + Asclepiadoideae], in that both are outgrowths of the stamen-corolla tube, then there is a potential synapomorphy for the larger group, or a parallelism if they do not form a single clade (Livshulz et al. 2007). There is quite a lot of variation in pollen morphology in Apocynaceae, independent of pollinarium formation. Alyxieae in particular have grains with large pores, and some species have remarkable barrel-like pollen grains, the pores forming the ends of the barrel (M. Endress et al. 2007a). Although the surface of the grains is often smooth, is can also be rugose or have projections (Nilsson 1990). Periplocoideae and Secamonoideae are reported to have T-shaped and tetragonal tetrads and simultaneous microsporogenesis, and rhomboidal tetrads are also reported from taxa with successive microsporogenesis (Safwat 1962; Omlor 1998; Nilsson et al. 1993; see also Matomoro-Vidal et al. 2014); when microsporogenesis is successive, the tetrads are linear. There has been considerable discussion about the nature of the paired nectaries of Vinca in particular, and because of their vasculature, etc., it has been suggested that they are modified carpels (e.g. Woodson & Moore 1938; Rao & Ganguli 1963; Fahn 1979); this is unlikely. When the carpels are connate, placentation may be axile or parietal (the latter, Allamanda, see Fallen 1985). Syncarpy seems to have evolved more than once in the family, it is congenital in Acokanthera and postgenital in Allamanda (Sennblad & Bremer 1996). The carpels may be collateral (Spichiger et al. 2002). In Secamone. Baissea, etc., the whole stigmatic head is glandular (Safwat 1962), but in many (?all) Asclepiadoideae there are five restricted glandular regions on the head. An endothelium has been reported in the ovules of Apocynaceae s. str. (Kapil & Tiwari 1978; Cronquist 1981), but it is absent according to Rohwer (1996); there are a few reports of obturators or various morphologies in the family (Morokawa et al. 2015).

Apocynaceae are a much-studied group. See M. Endress and Bruyns (2000), Leeuwenberg (1994), Albers and Meve (2002: enumeration of succulent taxa) and Livshulz et al. (2007), all general, and for a magnificent revision of southern African stapeliads, see Bruyns (2004). See also Aniszewski (2007: alkaloids), Demarco et al. (2006: laticifer type), Lens et al. (2009c: wood anatomy, to be integrated), Cremers (1973: growth of some lianes), Glück (1919: colleters), Leeuwenberg (1983: Plumerioideae), Swarupanandan et al. (1996: flowers of Asclepiadoideae, classification), Meve et al. (2009: floral morphology of Marsdenieae), Bruyns (2000) and Bruyns et al. (2012), flowers of stapeliads, Kunze (1990, 2005a: corona), Nilsson (1986), Sampson and Anusarnsunthorn (1990: Parsonsia), Verhoeven and Venter (1994, 2001), Van der Ham et al. (2001: Alyxieae), Vinckier and Smets (2002b: orbicules), van de Ven and van der Ham (2006: Melodinus, etc.), Van der Weide and Van der Ham (2012: Tabernaemontaneae), and Volkova and Severova (2015: Vinca), all pollen, P. Endress (1994b: much floral morphology, esp. Asclepiadoideae), Kunze (e.g. 1993, 1994, 1996) and Demarco (2014), all stamen development, Sennblad (1997: general), Erbar (2014: nectaries), Civeyrel et al. (1998: pollinaria variation), Omlor (1996: translator structure in Periplocoideae and Secamonoideae, 1998: floral morphology and testa anatomy), Albers and Meve (2001: karyology), Endress et al. (1983) and Shamrov and Gevorkyan (2010b: gynoecium), Andersson (1931), Anantaswamy Rau (1940b), and Venkata Rao and Rama Rao (1954), all embryology, and Hillebrand (1872: seed hairs - how different are the two coma types?). There is much information on Periplocoideae, Secamonoideae, and Asclepiadoideae at a site run by S. Liede-Schumann and U. Meve while F. d'Alessi and L. Viljoen provide information on stapeliads in particular; for Fockeeae, see Jankalski (2014).

Phylogeny. Both Rauvolfioideae and Apocynoideae are paraphyletic (Sennblad & Bremer 1996, 2002); see Livshultz et al. (2007) for the phylogeny of "Apocynoideae" and Simões et al. (2007a) for that of "Rauvolfioideae", particularly paraphyletic. The relationships of seven tribes in the latter are more or less clear, but those of the remaining five tribes remain to be established; there is good support for Aspidospermeae and Alstonieae as successively sister to all other Apocynaceae (Simões et al. 2007), and both tribes more or less lack uniseriate rays, a feature uncommon in other "Rauvolfioideae" (Lens et al. 2008b). For relationships in Vinceae, see Simões et al. (2016); Kopsia is sister to the rest, although taxa outside basal Apocynaceae were not included. Simões et al. (2010, see also 2006a) have clarified relationships within Tabernaemontaneae, i.a. circumscribing Tabernaemontana broadly to include Stemmadenia; major clades within that genus are correlated with geography. For a phylogeny of Alyxieae, M. Endress et al. (2007). Burge et al. (2013) clarified relationships within the much-cultivated Pachypodium. Z.-D. Chen et al. (2016) take a comprehensive look at Chinese Apocynaceae. recovering many of the relatiosnhips discussed here, although with a few differences, e.g. Nerieae are paraphyletic.

Apocynoideae, Periplocoideae, Secamonoideae, and Asclepiadoideae, i.e. basically the old Apocynoideae, Periplocoideae/Periplocaceae, and Asclepidaceae, form the APSA clade, relationships within which are being clarified. A question was whether or not Periplocoideae were immediately related to [Baisseeae [Secamonoideae + Asclepiadoideae]]; relationships could be [Periplocoideae [[Asian clade + New World clade] [Baisseeae [Secamonoideae + Asclepiadoideae]]], with the position of Rhabdadenia unclear (e.g. Livshulz 2010: perhaps 8 times the current amount of parsimony-informative data would solve the problem). Straub et al. (2014) examined plastome sequences of 13 taxa in the APSA clade, and from analysis of these data they suggested that that Periplocoideae were not immediately related to the old asclepiads; the relationships they obtained are followed above.

Parsonsia and Echites (Echiteae: Sennblad & Bremer 2002) are part of the New World clade, Mesechiteae. For phylogenetic relationships in Mesechiteae, see Simões et al. (2004, 2006b); in an earlier circumscription, the tribe was polyphyletic. There is small mostly African clade, Baisseeae, in which Dewevrella, with coiled filaments, is sister to the rest - and it is morphologically rather different from them (Livshultz 2009, esp. 2010). They are strongly supported as being sister to [Secamonoideae + Asclepiadoideae]. Below Baisseeae is a polytomy including a largely Asian clade (but including Apocynum) of ex-Apocynoideae, a largely American clade of that group, Rhabdadenia, and Periplocoideae (Livshultz et al. 2007; Livshulz 2010; see also Lahaye et al. 2007). Within Periplocoideae Phyllanthera is sister to the rest, although only the Australian species has been examined; pollinia seem to have evolved at least three times (Ionta & Judd 2007; Joubert et al. 2016: relationships slightly different; see also Venter & Verhoeven 2001).

Surveswaran et al. (2014) found that relationships within Asclepiadoideae were [Fockeeae [Eustephieae + Asclepiadeae] [Ceropegieae + Marsdenieae]], although support for the first pair was not very strong. Relationships within New World Asclepiadoideae have been clarified by e.g. Liede-Schumann (2005), Rapini et al. (2007) and Suilva et al. (2012: most genera of Metastelmatinae are not monophyletic). Vincetoxicum is not monophyletic (Yamashiro et al. 2004); Liede-Schumann et al. (2012) clarified relatioships in the whole Tylephorinae, to which it belongs. Relationships around Astephaninae are unclear (Liede 2001). Hoya and Dischidia (Marsdenieae) are fairly close (Livshultz et al. 2013: outline of relationships within the tribe), and could be separated by morphological features, possibly apomorphies, such as pollinarium morphology, inner guide rail presence/absence, and nectary position (Wanntorp & Kunze 2009). However, whether Dischidia is sister to or embedded within Hoya remains unclear (Wanntorp et al. 2014). Estimates of species numbers in these two genera in particular vary widely, although Hoya is particularly speciose; see also Wanntorp et al. (2006a, b, 2009) for phylogenies, Wanntorp and Forster (2007: floral morphology in general), Kunze and Wanntorp (2008a: corona and anther skirt) and Kunze and Wanntorp (2008b: focus on Hoya spartioidea). Relationships along the backbone of Hoya remain poorly resolved (Wanntorp et al. 2011a). For relationships within Asclepias, polyphyletic, see Goyder et al. (2007); Asclepias in the New World is sister to an Old World clade of Asclepiadoideae within which the Old World Asclepias are embedded, however, support for the two clades is not strong, and basal relationships within the Old World clade also have little support. A study focusing on New World Asclepias found that Trachycalymma was sister to both the Old and New World clades, although none of these relationships had much non-parametric bootstrap support (Fishbein et al. 2011); in Goyer et al. (2007) Trachycalymma was embedded within the Old World clade. For the delimitation and relationships of Cynanchum, see Liede and Kunze (2002), Liede and Täuber (2002) and especially Khanum et al. (2016). Within Ceropegieae relationships are complex, Ceropegia itself occurring all over the tree and Brachystelmia being embedded in it (Meve & Leide 2001, 2002a; Meve & Liede-Schumann 2007; Bruyns et al. 2015); the genera had been delimited using gross floral morphology. The stapeliads are monophyletic, but are embedded in Ceropegieae (Bruyns et al. 2014a, 2015). For the Gonolobus area, see Krings et al. (2008).

Overalll relationships in the extensive analysis by L.-L. Yang et al. (2016) are quite similar to those described above, and overall support values were quite high. There are a fea absences like Rhabdadenieae, unsurprising given the geographical focus (China) of the analysis, relationships between Odontadenieae and Echiteae were unclear, Periplocoideae were of uncertain position, and there was some support for a [Marsdenieae + Ceropegieae] clade in Asclepiadoideae.

Classification. The suprageneric classification here is based on that of M. Endress et al. (2007a and in particular 2014; see also Endress & Bruyns 2000; summary in Nazar et al. 2013); for subtribes, see M. Endress et al. (2014). No attempt has been made to develop a rational classification throughout the family, since this must await clarification of relationships between the basal clades, i.e. within the old Rauwolfioideae.

In general, generic limits need attention (see e.g. Liede & Täuber 2000; Liede et al. 2002; Rapini et al. 2003; Goyder et al. 2007l; Meve & Liede-Schumann 2007). For generic limits in Tabernaemontaneae, see Simões et al. (2010). Generic limits in Asclepiadoideae are particularly difficult, and current genera can seem to be distinguished by floral minutiae. Asclepias itself is definitely polphyletic, the New World clade including the type of the genus (Goyder et al. 2007), but morphology alone is not clarifying relationships too much; Goyder (2009) provisionally included even Trachycalymma (see above) in an admittedly unsatisfactorily circumscribed African Asclepias. Ceropegieae are another very difficult area, indeed, various genera are embedded within Caralluma, in turn embedded in Ceropegia (Meve & Leide 2001, 2002; Meve & Liede-Schumann 2007; Bruyns et al. 2010: see de Kock & Meve 2007 for a checklist). Bruyns et al. (2015: p. 50) noted that Surveswaran et al. (2009) "found that Brachystelma is not monophyletic and also that Ceropegia is not monophyletic unless Brachystelma and the stapeliads are included in it.". They found the same relationships, and seemed to be inclining to an enlarged Stapelia with around 670 species. For the circumscription of Sarcostemma, see Liede and Täuber (2000); it is included in Cynanchum, the limits of which have reasonably been drawn quite widely (Khanum et al. 2016). For genera in the Asclepiadoideae-Marsdenieae, see Omlor (1998) and Meve et al. (2009); to make Marsdenia monophyletic, the tribe, which includes Hoya, etc., would become monogeneric (Livshultz et al. 2013). Liede-Schumann et al. (2012) extend the limits of the Old World genus Vincetoxicum, which now includes Tylophora. For a very useful generic synonymy of Periplocoideae, Asclepiadoideae and Secamonoideae, see http://www.bio.uni-bayreuth.de/planta2/research/databases/delta_as/triblist.html

Thanks. I thank M. Endress for comments.