EMBRYOPSIDA Pirani & Prado

Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, 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, sporopollenin + laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae], >1000 spores/sporangium; nuclear genome size <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.

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]; 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; ycf2 gene in inverted repeat, mitochondrial trans- nad2i542g2 and coxIIi3 introns present; 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 apical meristem intermediate-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 very small [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).


Plant herbaceous, perennial, rhizomatous, growth sympodial; non-hydrolyzable tannins [(ent-)epicatechin-4] +, neolignans, benzylisoquinoline alkaloids 0, hemicelluloses as xylans; root apical meristem?; epidermis developed from outer layer of cortex; trichoblasts in atrichoblast [larger cell]/trichoblast cell pairs, the former further from apical meristem, in vertical files; endodermal cells with U-shaped thickenings; cork cambium [uncommon] superficial; stele oligo- to polyarch, medullated [with prominent pith], lateral roots arise opposite phloem poles; stem primary thickening meristem +; vascular bundles scattered, (amphivasal), vascular cambium 0 [bundles closed]; tension wood 0; vessel elements in roots with scalariform and/or simple perforations; tracheids only in stems and leaves; sieve tube plastids with cuneate protein crystals alone; stomata parallel to the long axis of the leaf, in lines; prophyll single, adaxial; leaf blade linear, main venation parallel, the veins joining successively from the outside at the apex and forming a fimbrial vein, transverse veinlets +, unbranched [leaf blade characters: ?level], vein/veinlet endings not free, margins entire, Vorläuferspitze +, base broad, ensheathing the stem, sheath open, petiole 0; inflorescence terminal, racemose; flowers 3-merous [6-radiate to the pollinator], polysymmetric, pentacyclic; P = T, each with three traces, median T of outer whorl abaxial, aestivation open, members of whorls alternating, [pseudomonocyclic, each T member forming a sector of any tube]; stamens = and opposite each T member [primordia often associated, and/or A vascularized from tepal trace], anther and filament more or less sharply distinguished, anthers subbasifixed, wall with two secondary parietal cell layers, inner producing the middle layer [monocot type]; pollen reticulations coarse in the middle, finer at ends of grain, infratectal layer granular; G [3], with congenital intercarpellary fusion, opposite outer tepals [thus median member abaxial], placentation axile; compitum +; ovule with outer integument often largely dermal in origin, parietal tissue 1 cell across; antipodal cells persistent, proliferating; fruit a loculicidal capsule; seed small to medium sized [mean = 1.5 mg], testal; embryo long, cylindrical, cotyledon 1, apparently terminal, with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial, plumule apparently lateral; primary root unbranched, not very well developed, stem-borne roots numerous, hypocotyl short, (collar rhizoids +); cotyledon with a closed sheath, unifacial [hyperphyllar], both assimilating and haustorial; no dark reversion Pfr → Pr; duplication producing monocot LOFSEP and FUL3 genes [latter duplication of AP1/FUL gene], PHYE gene lost.

[ALISMATALES [PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]]: ethereal oils 0; raphides + (druses 0); leaf blade vernation supervolute-curved or variants, (margins with teeth, teeth spiny); endothecium develops directly from undivided outer secondary parietal cells; tectum reticulate with finer sculpture at the ends of the grain, endexine 0; (septal nectaries +) [intercarpellary fusion postgenital].

[PETROSAVIALES [[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]]: cyanogenic glycosides uncommon; starch grains simple, amylophobic; leaf blade developing basipetally from hyperphyll/hypophyll junction; epidermis with bulliform cells [?level]; stomata anomocytic, (cuticular waxes as parallel platelets); colleters 0.

[[DIOSCOREALES + PANDANALES] [LILIALES [ASPARAGALES + COMMELINIDS]]]: nucellar cap 0; endosperm nuclear [but variation in most orders].

[LILIALES [ASPARAGALES + COMMELINIDS]]: (inflorescence branches cymose); protandry common.

[ASPARAGALES + COMMELINIDS]: style long; whole nuclear genome duplication [τ/tau event].

Age. This node has been dated to 118-116 m.y.a (Bremer 2000b; Leebens-Mack et al. 2005). Other estimates are ca 122 m.y. (Janssen & Bremer 2004), (112-)107, 98(-93) m.y. (Wikström et al. 2001) and ca 133.1 and 118.6 m.y. (Magallón & Castillo 2009); ages are around 159 m.y. in Paterson et al. (2004), ca 135.6 in Tank et al. (2015: Table S1), (126-)122(-98) m.y. in Merckx et al. (2008a), about 121 m.y. in Foster et al. (2016: q.v. for details), a mere 76.6 or 75.4 m.y. in Xue et al. (2012) and 88.9-78.2 m.y. in Good-Avila (2006), (130-)121(-116) or (121-)115(-110) m.y. (Hertweck et al. 2015: the former age is older than that of the [Liliales + The Rest] node), a group of similar estimates, 116-94 m.y. in Mennes et al. (2013, see also 2015), about 120-90 m.y. in S. Chen et al. (2013: conflicting estimates), and about 114.6 m.y.a. in Magallón et al. (2015), and finally (133.9-)123.6(-113.1) m.y.a. in Eguchi and Tamura (2016).

Evolution. Genes & Genomes. A genome duplication may be common to the monocots as a whole (Jiao et al. 2014), or at least to the clade [Asparagales + The rest] (Deng et al. 2015); the latter position for the placement of this τ/tau genome duplication event seems more likely (McKain et al. 2016; see also Olsen et al. 2016; H. T. Lee et al. 2016). P. Soltis and Soltis (2016) note that uncertainty over exactly where this event should be placed makes it difficult to think about any evolutionary implications it might have.

ASPARAGALES Link  Main Tree.

Chelidonic acid +, steroidal saponins 0 [exact position where?]; (velamen +), root hairs from unmodified rhizodermal cells; anthers longer than wide; microsporogenesis simultaneous; ovules many/carpel; seeds exotestal, tegmen not persistent; endosperm helobial; mitochondrial sdh3 gene lost. - 14 families, 1,122 genera, 36,205 species.

Age. Crown group Asparagales may be ca 125.3 m.y.o. (Tank et al. 2015: Table S2), ca 119 m.y.o. (Janssen & Bremer 2004) or (118-)112, 110(-106) m.y. (Hertweck et al. (2015; see also Givnish et al. 2015, 2016a), although Wikström et al. (2001: note topology) had suggested dates of 101-92 m.y.; Magallón and Castillo (2009) suggested ages of ca 112.6 m.y. and Bell et al. (2010) ages of (114-)103, 92(-83) m.y.; estimates are (127-)119(-101) m.y. in Merckx et al. (2008a), 96-93 m.y. or 113-63 m.y.a. in Mennes et al. (2013, 2015 respectively), 101-93 or 85.1 m.y. in S. Chen et al. (2013), about 109 m.y.a. in Magallón et al. (2015) and (125.8-)112.9(-98.4) m.y. in Eguchi and Tamura (2016). The age in Smith et al. (2008) is (95.6-)90.3(-85) m. years. The lowest suggested age seems to be 69-60 m.y.a. by Good-Avila et al. (2006).

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. Asparagales may have the highest diversification rate in the monocots, about the same as Poales, but in both the rate is little over half that of Lamiales, the angiosperm clade with the highest rate (Magallón & Castillo 2009); Magallón and Sanderson (2001) did not give estimates for the group. Within the clade, the diversity of Orchidaceae is remarkable, but to understand that diversity it makes more sense to focus on clades within Orchidaceae (e.g. Givnish et al. 2015; see below).

Asparagales are notably diverse in southern Africa, an estimate of some 2,550 species in five major clades growing there (Johnson 2010).

S. Chen et al. (2013) give age estimates for many nodes in Asparagales in particular, but differences between the two methods that they used were often substantial, the older ages (from BEAST) being about half as much again as the younger age (PATHd8) in a third or so of the cases.

Plant-Animal Interactions. Food plants of caterpillars of the [Heteropterinae-Trapezetinae-Hesperiinae] clade of skippers are common here, but most are found on Poaceae (Warren et al. 2009).

Bacterial/Fungal Associations. Asparagales commonly have Arum-type arbuscular mycorrhizae where the hyphae are intercellular, and also form coils, pelotons and particularly branched arbuscules within cells, while in Liliales these mycorrhizae are commonly Paris-type with intercellular hyphae that form coiled structures between the cells (see F. A. Smith & Smith 1997; Rasmussen & Rasmussen 2014).

Genes & Genomes. Asparagales have the greatest relative spread in genome sizes - 0.3-82.2 pg (1C: Leitch & Leitch 2013).

Chemistry, Morphology, etc. For pyrrolizidine alkaloids, scattered here, and homospermidine synthase (HSS), an early gene in the pathway that produces them, see Nurhayati et al. (2009), and for fructan sugar accumulation, quite common outside Orchidaceae, see Pollard (1982). The HSS gene had diverged considerably from the deoxyhypusine gene, from which it is derived, and Nurhayati et al. (2009) suggested that this was evidence of an ancient separation, although they were not sure where/when this happened. Storage mannans in the vegetative tissues are reported from Asphodelaceae-Asphodeloideae, Amaryllidaceae and Orchidaceae; they are uncommon elsewhere (Meier & Reid 1982). There is no starch in the chloroplasts of guard cells of members of Amaryllidaceae, Iridaceae, and "Liliaceae" (= Allium) and no chloroplasts at all in those of Paphiopedilum Orchidaceae (D'Amelio & Zieger 1988; Willmer & Fricker 1996).

Three-trace tepals are found in Orchidaceae, Amaryllidaceae-Amaryllidoideae and -Agapanthoideae, Iridaceae, Asphodelaceae-Asphodeloideae (but not Kniphofia, Ashpodelus) and -Hemerocallidoideae, Asparagaceae-Agavoideae; one-trace tepals in Amaryllidaceae-Allioideae and Asparagaceae-Nolinoideae (but not Maianthemum stellatum), -Aphyllanthoideae, and -Asparagoideae. Asparagaceae-Scilloideae have tepals with both one and three traces, Urginea even having five traces in the outer whorls (see especially Chatin 1920). Where changes in microsporogenesis are to be placed on the tree is not clear. Furthermore, Rudall (2001a, see also 2002, 2003a) included an inferior ovary as a synapomorphy of the order, noting that in "higher" Asparagales there might be a reversal to superior ovaries that is associated with the presence of infralocular septal nectaries (as in Xanthorrhoea and Johnsonia (Asphodelaceae-Xanthorrhoeoideae and -Hemerocallidoideae). However, since inferior ovaries are scattered through the "lower" Asparagales, fitting ovary evolution to the tree is difficult; ovary position seems a much more flexible character here (and elsewhere) than it has generally been given credit for.

For flavonoids, see Williams et al. 1988), for general morphology, see Rudall (2003a), for root morphology, see Kauff et al. (2000), for cladodes, see Schlittler (1953b), for inflorescences, see Schlittler (1953a), for pollen of Japanese representatives, see Handa et al. (2001), for ovule and seed, see Shamrov (1999a) and Oganezova (2000a, b), for cytology, see Tamura (1995), and for the distribution of taxa with phytomelan and/or with baccate fruits, see Rasmussen et al. (2006).

Phylogeny. For a discussion about the relationships of Asparagales, see the Petrosaviales page.

The tree (below) of relationships within Asparagales is based largely on the analyses in Chase et al. (2000a) and Fay et al. (2000: successive weighting). These studies differ little in detail, although the analysis of Fay et al. (2000) hardly suprisingly had more nodes in the core Asparagales with strong support; they are consistent with relationships in Chinese Asparagales as detailed in Z.-D. Chen et al. (2016) and the relationships in McLay and Bayly (2016), although the focus of the latter was Asphodelaceae. For the [Amaryllidaceae + Agapanthaceae] clade, see Meerow et al. (2000b), and relationships between Aphyllanthaceae, Themidaceae and Hyacinthaceae might be better represented as trichotomy (see also S. Chen et al. 2013); these families are now subsumed in a broadly-drawn Amaryllidaceae and Asparagaceae respectively. The relationships in McPherson and Graham (2001) and D.-K. Kim et al. (2012) are largely congruent with those in the tree below, although their sampling is poorer and more geographically constrained.

Understanding the relationships between Boryaceae and Orchidaceae is important. Boryaceae have been placed as sister to Orchidaceae (e.g. Chase et al. 1995a; McPherson & Graham 2001), although with rather weak support. Janssen and Bremer (2004) found the relationships [[Boryaceae, Blandfordiaceae, etc.] [Orchidaceae [Ixoliriaceae [Tecophilaeaceae [Doryanthaceae + The Rest]]]]], while Orchidaceae were embedded in a Boryaceae-Hypoxidaceae clade (Li & Zhou 2007), but again, with little support. In Wikström et al. (2001) Orchidaceae were sister to Hypoxidaceae. Seberg et al. (2012: mitochondrial and chloroplast data agreed only after removing edited mitochondrial sites) largely recovered the topology found by earlier workers; mitochondrial data provided little support for the backbone of the tree.

Recent work suggests that Orchidaceae are sister to all other Asparagales (e.g. 76% bootstrap support in Graham et al. 2006; about the same in Givnish et al. 2006b; stronger [96-99%] in Pires et al. 2006: good sampling, seven genes from two compartments; Chase et al. 2006; S. Chen et al. 2013). There was more or less strong support for the [Boryaceae, Blandfordiaceae et al.] clade in these analyses. In some phylogenetic reconstructions of Hilu et al. (2003) Asparagales were paraphyletic, Orchidaceae being separate from the rest. Rudall (2003a: morphological data) suggested that there was a close relationship between Hypoxidaceae and Orchidaceae in particular, and also between Boryaceae and Blandfordiaceae and Iridaceae and Doryanthaceae. All in all, the topology [Orchidaceae [[Boryaceae, Blandfordiaceae et al., = astelioids] [all other Asparagales]]], seems the best hypothesis. This affects the characterisation of Asparagales, since some characters previously considered to refer to the clade as a whole move to the next node up (c.f. versions 6 and younger of this site).

Within the stelioids, a clade [Asteliaceae [Lanariaceae + Hypoxidaceae]] was recovered by S. Chen et al. (2013). while in Chase et al. (2006) Boryaceae were placed immediately above the Blandfordiaceae et al. clade, albeit with very little support. The clade [[Ixoliriaceae + Tecophilaeaceae] [Doryanthaceae [Iridaceae [Xeronemataceae + The Rest]]]] is strongly supported in analyses using data from four plastid genes (Fay et al. 2000; see also Chase et al. 2000a; Soltis et al. 2007a), but no morphological characters have yet been found for it. The positions of [Ixoliriaceae + Tecophilaeaceae] and Doryanthaceae are reversed in Kim et al. (2011) and in Fig. 2 in S. Chen et al. (2013), although in their Fig. 3 the three families are shown forming a clade [Doryanthaceae [Ixoliriaceae + Tecophilaeaceae]], and they do have a few features in common.

Classification. There have been suggestions that Orchidaceae should be placed in their own order, either because of their age and/or diversity and morphology (e.g. Eguchi & Tamura 2016).

Previous Relationships. Dahlgren et al. (1985) took important steps in reorganizing the relationships of "lily-like" monocots. They recognized two groups, Asparagales and Liliales, which were separable by features including patterning of the tepals and absence of phytomelan, both features of their Liliales. However, they still included Iridaceae and Orchidaceae in Liliales.

Includes Amaryllidaceae, Asparagaceae, Asphodelaceae, Asteliaceae, Blandfordiaceae, Boryaceae, Doryanthaceae, Hypoxidaceae, Iridaceae, Ixioliriaceae, Lanariaceae, Orchidaceae, Tecophilaeaceae, Xeronemataceae.

Synonymy: Asparagineae J. Presl, Asphodelineae Thorne & Reveal, Hyacinthineae Link, Iridineae Engler, Scillineae J. Presl - Agavales Hutchinson, Alliales Berchtold & J. Presl, Amaryllidales Link, Apostasiales Martius, Asphodelales Doweld, Asteliales Dumortier, Gilliesiales Martius, Hypoxidales Martius, Iridales Rafinesque, Ixiales Lindley, Narcissales Dumortier, Orchidales Rafinesque, Tecophilaeales Reveal, Xanthorrhoeales Reveal & Doweld

ORCHIDACEAE Jussieu, nom. cons.   Back to Asparagales

Mycorrhizal herbs, protocorms +, mycoheterotrophic; flavone C-glycosides, flavonols +, chelidonic acid?; conical SiO2 bodies in stegmata; stomata frequently tetracytic; leaf vascular bundle sheaths with fibres, (also fibre bundles in leaves); flowers rather weakly monosymmetric, resupinate [median outer T adaxial; flowers described as if upside-down]; T free, lateral out T first to develop, median member the last, median [abaxial] inner T differentiated [= labellum]; A 3, [median of outer whorl and laterals of inner whorl], basally adnate to style; endothecial thickenings annular; tapetal cells uninucleate; pollen with elastoviscin; ovary inferior, septal nectaries 0, placentatation axile, placentae bilobed [?here], style solid [?all], stigmas commissural, wet; ovules ca 1500+/carpel, parietal tissue none, funicle not vascularized; fruit dehiscing laterally, six valves, (indehiscent, ± baccate), T deciduous in fruit; seeds minute, dust-like; endosperm barely developing, none at maturity, embryo minute, undifferentiated [radicle 0], suspensor often haustorial (and branched); x = 7?

Orchidaceae tree

Ca 880[list]/27,800 - five subfamilies below. World-wide. [Photo - Flower]

Age. Crown group Orchidaceae have been dated to ca 111 m.y. (Janssen & Bremer 2004) or (121-)93.7(-75) m.y.a. (Chomicki et al. 2014c). The estimates of Ramírez et al. (2007: calibration by Miocene Goodyerinae pollinaria in amber, see esp. Supplementary Table) are somewhat younger at (90-)84-76(-72) m.y., and they were recalculated by Gustafsson et al. (2010) as (105-)80(-56) m.y. ago. Other crown group estimates include (105-)80-77(-56) m.y. (Gustafsson et al. 2010: BEAST), while ages in Givnish et al. (2015, 2016a), at (99.5-)90(79.7) m.y., i.e. with a ca 20 m.y. "fuse", and Bouetard et al. (2010) were slightly older, and the youngest are at (82-)68(-54) or ca 51.6 m.y. in S. Chen et al. (2013). Although Janssen and Bremer (2004) did not place Orchidaceae sister to the rest of the order, its stem-group origin was near the beginning of divergence within it at ca 119 m.y. ago.

1. Apostasioideae Horaninov


Chemistry unknown; roots tuberous, tubers with irregular papillae, velamen uniseriate; pith with scattered vascular bundles; vessel elements in roots often with simple perforation plates, (vessels in stem +); leaves spiral, vernation plicate; (flowers not resupinate - Apostasia); T develop from a ring primordium, lateral members of inner T develop first, T apiculate, carinate [prominent midrib], (labellum 0 - Apostasia); (A 2, staminode +/0 - Apostasia); pollen surface reticulate, colpus operculate; stigma lobes spreading; micropyle bistomal; (embryo sac bisporic, the spores chalazal, 8-celled [Allium type] - Neuwiedia); seeds dark in colour, endotestal, exotesta with cuticular layer, cells isodiametric, sclerified [Neuwiedia], outer periclinal walls collapsing; n = 24.

2/15. Sri Lanka, N.E. India to N.E. Australia, Japan (map: from Pridgeon et al. 1999).

Age. Estimates of the age of crown-group Apostasioideae are (54-)49-45(-41) m.y.o. (Ramírez et al. 2007), or (66-)43(-23) and (61-)41(-23) m.y.o. (Gustafsson et al. 2010).

Synonymy: Apostasiaceae Lindley, Neuwiediaceae Reveal & Hoogland

[Vanilloideae [Cypripedioideae [Orchidoideae + Epidendroideae]]]: C-glycosyl flavones, (saponins), 6-hydroxy flavonols +; vessel elements with scalariform perforation plates; (stegmata 0); leaves spiral or two-ranked; flowers strongly monosymmetric; (tepal nectaries +), abaxial outer tepal develops after inner whorl, labellum strongly differentiated, develops before other members of the inner whorl; the style and A almost completely congenitally fused [column, = gynostemium], anthers to 2x as broad as long; pollen sticky; placentation parietal, hairs/papillae on inside of carpel wall, stigma asymmetric [lateral lobes, + part median lobe]; ovules not fully developed at pollination, (embryo sac 6-nucleate); fertilization may take some months; exotestal cells ± elongated; radicle 0.

Age. The age of this node is around 71 m.y. (Gustafsson et al. 2010) or (92.9-)84(-74.4) m.y. (Givnish et al. 2015, 2016a).

2. Vanilloideae Szlachetko


Plant (monopodial), often viny, (echlorophyllous, mycoheterotrophic, associated with ECM fungi); (lignin with catechyl units - Vanilla); velamen +, plant glabrous; stomata notably variable; (lamina venation reticulate); (inflorescence axillary); (calyculus +); T often carinate, (margins of labellum fused with column - some Vanilleae); A 1 [= median [abaxial] member of outer whorl], staminodes 2 [= lateral members of inner whorl], anther incumbent [bent forward] by massive expansion of the apical column/connective; "pollinia" +, soft [not highly organized], viscidium 0; pollen inaperturate[?], (polyporate), (in tetrads), smooth or not; (placentation axile), rostellum [ridge, part of median stigmatic lobe] +; (T persistent in fruit), (fruit baccate); seeds often relatively large, (winged), (spherical, crustose, [testal - outer parietal wall well developed], tegmen persisting), (exotesta with cuticular layer); endosperm 0 or to 16-nucleate; n = 9, 10, 12, 14-16, 18, etc.

14/245: Vanilla (105), Cleistes (64). Pantropical, esp. Asia; Australia, some N. America (map: from Pridgeon et al. 2003).

Age. Crown group Vanilloideae are (76-)71-65(-61) m.y.o. (Ramírez et al. 2007), or (79-)58(-39) m.y.) and (72-)57(-43) m.y. as recalculated by Gustafsson et al. (2010), while ca 71 m.y.a. is the estimate in Bouetard et al. (2010) and around abour 77 m.y. in Givnish et al. (2016a).

Synonymy: Vanillaceae Lindley

[Cypripedioideae [Orchidoideae + Epidendroideae]]: exotesta lacking cuticular layer.

Age. The age of this clade is estimated at 37-26 m.y. by Wikström et al. (2001), (69-)48, 42(-23) m.y. by Bell et al. (2010), around 69-68 m.y. by Gustafsson et al. (2010) and (87.4-)76(-64.6) m.y. by Givnish et al. (2015, 2016a).

3. Cypripedioideae Kosteletzky


(Plant epiphytic, epilithic); root with persistent hairs, (velamen +), (pith 0 - some Cypripedium); stem bundles amphivasal; stomata anomocytic - Cypripedium; leaf vernation conduplicate or plicate; 2 abaxial T of outer whorl connate, labellum saccate; A 2 [= lateral members of inner whorl], (pollinia +), staminode single, conspicuous [= median member of outer whorl]; tapetal cells binucleate; microsporogenesis successive?; pollen sulcate, ± smooth [psilate], (foveolate), (in tetrads), sticky or not; stigma lobes spreading, median lobe largest; (micropyle bistomal); embryo sac bisporic [chalazal dyad], eight-celled [Allium-type]; (T persistent in fruit); (outer periclinal wall of testa sclerified - Selenipedium); n = 9 or more.

5/170: Paphiopedilum (86), Cypripedium (51). Mostly (warm) temperate N. Hemisphere, East Malesia and tropical South America (S. India) (map: from Hultén 1958; Pridgeon et al. 1999). [Photo - Flower]

Age. Crown group Cypripedoideae are (54-)49-44(-39)/(66-)43-41(-23) m.y.o. (Ramírez et al. 2007), but recalculated as (49-)31(-17) m.y.) and (50-)33(-19) m.y. by Gustafsson et al. (2010), while from Fig. 1 in Givnish et al. (2016a) their age is around 63 m. years.

Synonymy: Cypripediaceae Lindley

[Orchidoideae + Epidendroideae]: (plant echlorophyllous, mycoheterotrophic, associated with ECM fungi); leaves withering on the plant; floral primordium tranversely elliptic-oval; labellum initiated first; A 1 [= median [abaxial] member of outer whorl], sporangia 2 [?level], (staminodes 2 [from outer whorl]); microsporogenesis simultaneous [tetrads tetrahedral]; pollinia +, attached to sticky viscidium, pollinium/pollinarium stalk variously formed; pollen in tetrads (monads), inaperturate, (porate or ulcerate); median [adaxial] carpel developed before the others, rostellum + [ridge, part of median stigmatic lobe, viscidium is also part of it]; T persistent in fruit; tegmen not persisting; endosperm not developing at all; n = 9 or more [19 common].

Age. The age of this node is estimated to be around 59-51 m.y.a. (Gustafsson et al. 2010) or (73.7-)64(-54.8) m.y. (Givnish et al. 2015, 2016a).

4. Orchidoideae Eaton


Root tubers +/0 (fleshy rhizomes +); (glucomannans +); (velamen +), (exodermis/tilosomes +); (amyloplasts with numerous minute starch grains [= spiranthosomes]); sclerenchyma in leaf [as fibre bundles or associated with vascular bundles] and stem rare; stomata anomocytic; leaves usu. spiral, soft, herbaceous; anther erect (incumbent), apex acute, staminodes of inner whorl reduced; pollinia soft/sectile, (hamulus + [= pollinium stalk, from recurved apical part of rostellum]), (caudicles + [= pollinium stalk, from basal extension of pollinia]); n = 12-24 [x = 7?].

208/3755: [CR = Cranichideae, DI = Diurideae, OR = Orchideae] Habenaria (OR: 840), Caladenia (DI: 270), Platanthera (OR: 136), Pterostylis (CR: 215), Disa (OR: 182), Cynorkis (OR: 156), Microchilus (CR: 137), Corybas (DI: 132), Prasophyllum (DI: 131), Thelymitra (DI: 110), Peristylus (OR: 105), Satyrium (OR: 86), Disperis (OR: 78), Cyclopogon (CR: 83), Pelexia (CR: 77), Zeuxine (CR: 74), Diuris (DI: 70), Ponerorchis (OR: 55), Cheirostylis (CR: 53), Sarcoglottis (CR: 48), Vrydagzynea (CR: 43). World-wide, esp. temperate (map: from Pridgeon et al. 2001, 2003; distribution in N. Asia and N. North America unclear).

Age. Crown group Orchidioideae are (63-)58, 52(-48) m.y.o. (Ramírez et al. 2007), or, as recalculated by Gustafsson et al. (2010), (67-)50(-34) m.y. and (64-)53(-42) m.y. old.

Synonymy: Neottiaceae Horaninow, Limodoraceae Horaninow, Liparidaceae Vines, Ophrydaceae Vines

5. Epidendroideae Kosteletzky


Epiphytes common, plant fleshy [stems, leaves], (monopodial); roots (with pneumathodes), (the main photosynthetic organs of the plant - Vandeae); (pyrrolizidine alkaloids +); velamen + (0), tilosomes +/0; (SiO2 bodies +, conical); bicellular mucilage-secreting floral hairs +; stomata often paracytic; stems thick; leaves usu. 2-ranked, vernation conduplicate (plicate), (unifacial, terete), (two-ranked and isobifacial), (articulated and deciduous above sheathing base); inflorescence axillary [?all]; anther incumbent [bent forward by column elongation, or by very early anther bending (vandoids)], (strongly convex), with beak, operculate; endothecial thickenings often other than annular; (tegulum + [= pollinium strap formed from epidermis (and subjacent cell layers) of rostellum] - vandoids); pollinia hard (soft/sectile), clavate, with a waxy surface; (inside of carpel wall with hairs); (cotyledon visible); n = 5+.

650/21,600 (14 tribes: AR = Arethuseae, CY = Cymbidieae, EP = Epidendreae, MA = Malaxideae, NEO = Neottieae, PO = Podochileae, SO = Sobralieae, VA = Vandeae): Bulbophyllum (MA: 1870), Dendrobium (MA: 1515), Epidendrum (EP: 1425), Lepanthes (EP: 1090), Stelis (EP: 885), Maxillaria (CY: 665), Pleurothallis (EP: 555), Masdevallia (EP: 595), Liparis (MA: 430), Oberonia (MA: 325), Oncidium (CY: 315), Dendrochilum (AR: 280), Crepidium (MA: 260), Eria (PO: 240), Polystachya (VA: 240), Calanthe (CO: 220), Angraecum (VA: 225), Phreatia (PO: 215), Telipogon (CY: 205), Coelogyne (AR: 200), Eulophia (CY: 200), Malaxis (MA: 185), Taeniophyllum (VA: 190), Octomeria (EP: 160, Appendicula (PO: 150)), Catasetum (CY: 180), Encyclia (EP: 170), Thrixspermum (VA: 165), Anathallis (EP: 155), Ceratostylis (PO: 150), Sobralia (SO: 150), Cyrtochilum (CY: 140), Dracula (EP: 130), Acianthera (EP: 120), Glomera (AR: 130), Dichaea (CY: 120), Gomesia (CY: 120), Prosthecea (EP: 120), Cattleya (EP: 115), Trichosalpinx (EP: 115) , Elleanthus (SO: 110), Pinalia (PO: 105), Platystele (EP: 105), Agrostophyllum (EP: 100), Specklinia (EP: 100), Cleisostoma (VA: 80), Comparettia (CY: 80), Mormodes (CY: 80), Trichotosia (PO: 80), Brachionidium (EP: 75), Gongora (CY: 75), Vanda (VA: 75), Cymbidium (CY: 70), Kefersteinia (CY: 70), Phalaenopsis (VA: 70), Scaphyglottis (CY: 70), Trichoglottis (VA: 70), Trichocentrum (CY: 70), Nervilia (NER: 67), Campylocentrum (VA: 65), Neottia (NEO: 65), Brassia (CY: 64), Podochilus (PO: 62), Gastrodia (GA: 60), Coryanthes (CY: 60), Kefersteinia (60), Stanhopea (CY: 60), Sophronitis (60), Aerangis (VA: 58), Gastrochilus (VA: 56), Notylia (CY: 56), Dryadella (EP: 55), Ornithidium (MA: 55), Ornithocephalus (CY: 55), Porroglossum (EP: 53), Restrepia (EP: 53), Octarrhena (PO: 52), Fernandezia (CY: 51), Epipactis (NEO: 50). More or less world-wide, but most diverse in the tropics; rather poorly developed in Australia (map: from Pridgeon et al. 2005).

Age. Crown group Epidendroideae are estimated to be (67-)59, 51(-44) m.y.o. (Ramírez et al. 2007), or recalculated as (60-)44(-29) m.y. and (62-)49(-38) m.y. (Gustafsson et al. 2010) or ca 48 m.y. (Givnish et al. 2016a); other estimates include (115-)97.7(-83) m.y. for Epidendreae alone (Sosa et al. 2016, q.v. for discussion).

Synonymy: Pycnanthaceae Ravenna

Evolution. Divergence & Distribution. Iles et al. (2015) give dates for three fossils reliably placed within Orchidaceae.

We still know rather little about the origin and biogeography of the family (see also Chase 2003). Givnish et al. (2016a) suggested that the family originated in Australia ca 112 m.y.a. and then spread via Antarctica to South America where Vanilloideae and Cypripedioideae originated by 64 m.y. ago. Ramírez et al. (2007) also suggested that the subfamilies had diverged by the end of the Cretaceous, ca 65 m.y.a. (see also Givnish et al. 2015, 2016a), or perhaps slightly later in the early Palaeocene, and that orchid radiation has been a Caenozoic phenomenon; dates suggested by Gustafsson et al. (2010) are somewhat younger, major diversification perhaps occurring during the cooler period at the end of the Eocene and into the Oligocene rather than during the thermal maximum earlier in the Eocene (c.f. Ramírez et al. 2007).

Despite the minute size of orchid seeds, long distance dispersal (l.d.d.) is not notably common (c.f. Vollering et al. 2015). However, Givnish et al. (2016a) estimated hat there had been around 73 l.d.d. events, even if the distributions of over 97% of orchid species are restricted to single continents. Indeed, there can be surprisingly low genetic differentiation between orchid populations, despite the possibility for l.d.d. of the seeds and resultant founder effects (Phillips et al. 2012), although epiphytic taxa in tropical mountains may show quite a bit of local genetic divergence (Givnish et al. 2015 for literature). There are a few exceptions where l.d.d. does seem to have occurred. Thus Bouetard et al. (2010) estimated that crown group Vanilla started to diversify ca 34 m.y.a., at least three instances of l.d.d. being needed to explain its present distribution, while l.d.d. seems also to be quite common in Spiranthes, S. romanzoffiana occuring on both sides of the Atlantic, movement having been from west to east (Dueck et al. 2014 and refs). Givnish et al. (2016a) discuss the biogeography and diversification rates of the family in some detail, emphasizing the role l.d.d. has played, and also the importance of the evolution of pollinia, the epiphytic habit and invasion of the northern Andes by the pleurothallid orchids.

Endress (2011a) thought that the inferior ovary in Asparagales might be a key innovation, although where this feature should be placed on the tree is unclear - perhaps here is one place. The presence of pollinia is another feature that he mentioned; this is probably best placed as a synapomorphy of the [Orchidoideae + Epidendroideae] clade. Indeed, much floral variation in Orchidaceae is at one level a series of remarkably intricate variations on a rather limited theme. Most species have a single anther, a labellum, a very similar gynoecium, etc., with variation centred on the pollinaria and labellum. For details on the distinctive pollinaria of many epiphytic Epidendroideae, see Freudenstein and Chase (2015), who noted that "vandoid" anthers may increase pollinator specifity and so promote diversification.

Gravendeel et al. (2004 and references; see also Peakall 2007) list the numerous hypotheses that have been advanced to explain the diversity of Orchidaceae, not all mutually exclusive. These include pollinator specialization, niche partitioning, habitat fragmentation, and wide dispersal of the seeds. Orchid diversity is most often attributed to the nature of the association of the plant with its pollinator, as is discussed below. Some of the distinctive features of the family seem to be biologically connected. Thus pollinia ensure the fertilization of numerous ovules, the minute seeds that result are usually devoid of endosperm or a differentiated embryo, and the obligate mycoheterotrophy of the young plant may compensate for the absence of seed reserves and undifferentiated embryo (Johnson & Edwards 2000 in part; Eriksson & Kainulainen 2011). A genome duplication shared by all orchids has been implicated in the evolution of many of the adaptive traits found in the family (Unruh et al. 2016).

However, there is no simple story. Orchidaceae, with around 27,800 species, are sister to the rest of Asparagales, which have only ca 7,100 species (c.f. Sargent 2004: Orchidaceae compared with Hypoxidaceae - only 100-220 species!). Indeed, these other Asparagales could perhaps be considered vegetatively and even florally more diverse than Orchidaceae, although it is hard to compare such things; Burleigh et al. (2006) suggest that by some measures Orchidaceae do show a notable increase in complexity. But continuing the numbers game, Asparagales as a whole, with around 34,600 species, are sister to commelinids, which have some 22,750 species. Within Orchidaceae, clades of 14, 245, and 170 species are successively sister to the rest, so suggesting a rather more complicated story (Givnish et al. 2015; see also in part Smith et al. 2011). Indeed, features like shifts to the epiphytic habit and the associated adoption of CAM photosynthesis, features of the crown Epidendroideae, are as likely to have been as important in orchid diversification as anything else (Gravendeel et al. 2004; Givnish et al. 2015; see also below). The highly speciose and commonly epiphytic-CAM crown Epidendroideae include around 19,560 species (figures from Pridgeon et al. 2005, 2009, 2014), i.e., about two thirds of the species in the whole family. Tropical species richness is highest in montane habitats, usually in the 1,000-2,000 m zone although in the 2,000-3,000 m zone in New Guinea (Vollering et al. 2015), and the orchids involved are largely epiphytic members of the core Epidendroideae (Givnish et al. 2015, 2016a).

Normally neither orchids nor pollinating insects are diverse on oceanic islands, but angraecoid orchids are surprisingly diverse on the Mascarene islands, and Réunion in particular also has a diverse insect fauna (Micheneau et al. 2008).

In the largely Old World and very diverse Bulbophyllum (Epidendroideae) the few (ca 60) New World species form a clade sister to the African taxa, the overall geographical pattern being [S. E. Asia [Madagascar [Africa [Africa + New World]]], and it is in Southeast Asia that the genus may have initially evolved (Gravendeel et al. 2004; Smidt et al. 2011; esp. B. Gravendeel, E. de C. Smidt, G. Fischer & J. J. Vermuelen in Pridgeon et al. 2014), with some 500 species in New Guinea alone. Bytebeier et al. (2011) note that about half the 180 species of the tuberous Disa (Orchidoideae) are restricted to the Cape Floristic Region, and they moved into subalpine/grassy habitats where they often flower immediately after fires, a habit that has been dated to around 12.9 m.y.a. (Bytebeier et al. 2011).

Ecology & Physiology.

Fungi and Orchids.

The obligate association of orchids with mycorrhizal saprotrophic fungi, mostly basiodiomycetes, is central to understanding the ecophysiology of the orchid plant (Rasmussen et al. 2015 for a recent review; see also Bacterial/Fungal Relationships). The fungal hyphae form intracellular pelotons, complex coils of hyphae, inside the plant cells, and these may be digested by the host. Establishment of this association is integral to the successful establishment of the seedling. The sometimes rather protracted obligate and at least initially echlorophyllous mycoheterotrophic phase of the young plant compensates for the absence of reserves in the minute seeds, and here the fungus-plant association does not appear to be antagonistic (Rasmussen 1995; Johnson & Edwards 2000 in part; Eriksson & Kainulainen 2011; Leake & Cameron 2012; Perotto et al. 2014; Rasmussen & Rasmussen 2014). The plant-fungal association results in the formation of a protocorm (Peterson et al. 1998) which may have a very distinctive morphology; although it lacks roots, it may have tufts of root hairs (Weber 1981; Bustam et al. 2014), and the root hairs ("rhizoids") are sometimes described as being branched (Rasmussen ?1999). Light commonly inhibits germination, even in epiphytic species (Rasmussen et al. 2015). A few orchids can germinate in the absence of a fungus, and in vitro germination of several terrestrial Australian orchids could be as effective on variously doctored asymbiotic media as on the standard symbiotic medium (Bustam et al. 2014).

Which came first, the dust seeds or the mycoheterotrophic association? This is almost a chicken-or-egg question, although Rasmussen and Rasmussen (2014) suggest that a developing association with ECM fungi was the spur. A variety of fungi, including the form genus Rhizoctonia, the anamorph stage of several quite unrelated basidiomycetes, form the initial fungus-orchid association, later on, specificity may be higher (Rasmussen & Rasmussen 2014). Sebacinales (basidiomycetes) clade B fungi, which are not ECM but are saprophytic and endophytic, are also involved, as are some clade A ectomycorrhizal (ECM) Sebacinales, and the association may last the life of the orchid (Hynson et al. 2012). Sugars and nitrogen move from the fungus to the orchid (Zimmer et al. 2007; Kuga et al. 2014). Orchid fungi that are saprotrophic can break down cellulose, but not lignin, and nutrients moving into the orchid come from the saprotrophic activities of the fungus (Dearnaley et al. 2012; Kohler et al. 2015; Teixeira da Silva et al. 2015 for references).

Details of fungus-orchid associations in Apostasioideae were until recently unclear. Here the ECM basidiomycete Tulasnella is involved, a genus also found in Cypripedium, etc. (Kristiansen et al. 2004; see also Yukawa et al. 2009; Roche et al. 2010). The fungus is found in stomatiferous root tubercules, and these may make the plant better able to deal with wet conditions (Stern & Warcup 1994). Interestingly, seeds of Apostasioideae are rather larger than those of other orchids.

Some kind of fungal orchid association in the adult stage is pervasive, and there may be a switch in fungal partners from the juvenile stage (e.g. Y.-I. Lee et al. 2015; Rasmussen et al. 2015 and references). Most adult orchids are autotropic, fixing all their own carbon, others are mixotropic, obtaining some carbon from the fungus (or the fungus may obtain carbon from the orchid), while mycoheterotrophic orchids lack chlorophyll and are totally dependent on the fungus for all carbon (and nitrogen); for a review, see Dearnalay et al. (2012; also Girlanda et al. 2011; Oberwinkler et al. 2013; Perotto et al. 2014). The part of the plant that hosts the fungus can vary (Ramsay et al. 1986). Tulasnella is associated with a number of adult orchids, these are autotrophic (Summer et al. 2012; Ogura-Tsujita et al. 2012). Indirect associations with trees are known from other than mycoheterotrophs (e.g. Bidartondo & Read 2008; see also Bidartondo et al. 2004: partial mycoheterotrophy), and here there can be bi- or unidirectional movement of carbon and nitrogen between chlorophyllous orchids and their fungi (e.g. Bidartondo et al. 2004; Cameron et al. 2008; Hynson et al. 2009a).

There are some 210 species of more or less echlorophyllous mycoheterotrophs (= holomycotrophs) in Orchidaceae, almost half of all mycoheterotrophs, and they have evolved some 30 or more times there (Molvray et al. 2000; Merckx & Freudenstein 2010; Freudenstein & Barrett 2010). They are most common in ground-dwelling Epidendroideae, where about 1 in 10 species is a mycoheterotroph (Freudenstein & Barrett 2010). Members of the Hexalextris spicata complex (Epidendreae) are each associated with different members of the ECM Sebacinales subgroup A (Kennedy et al. 2011). Several species of Russula form both ECM associations with adjacent trees and endomycorrhizal associations with Corallorhiza (Epidendroideae) (Taylor & Bruns 1999; see also Kinoshita et al. 2016: Gastrodia), and the tree then is the ultimate source of the orchid's carbon (see also Dearnaley 2007). Yagame et al. (2016) suggested that in Neottia there has been an evolutionary shift from associations with saprophytic/endophytic Sebacinales group B fungi found in the autotrophic taxa to associations with group A fingi in the echlorophyllous mycoheterotropic taxa. The Australian Rhizanthella (Orchidoideae-Diuridae) is a subterranean holomycotroph, the flowers even opening underground (Delannoy et al. 2011); it forms an association with the ECM fungi of Meleleuca uncinata (Rasmussen et al. 2015 and references). In Cymbidium (Epidendroideae) the evolution of mixotrophy and then mycoheterotrophy depends on the establishment of associations between the orchids and ECM fungi (Ogura-Tsujita et al. 2012); mycoheterotrophic and leafy taxa can hybridize (Cymbidium macrorhizon X C. ensifolium : Ogura-Tsujita et al. 2014). Non-mycorrhizal but lignin-decaying fungi like the basidiomycete Mycena (Mycenaceae) are also involved in such associations; Mycena supports the fully mycoheterotrophic Gastrodia confusa (Epidendroideae) in the manner to which it has become accustomed (Ogura-Tsujita et al. 2009 and references), and saprotrophic fungi other than Rhizoctonia are commonly associated with mycoheterotrophic orchids on Taiwan (Y.-I. Lee et al. 2015: ECM fungi only sometimes involved). The identity of the fungal associate may change with the establishment of full mycoheterotrophy (Hynson & Bruns 2010). Tropical holomycotrophs tend to be associated with saprotrophic fungi (Garbaye 2013).

Any connection between the specificity of the mycorrhizal association and the diversification of the family (Otero & Flanagan 2006) or even speciation in mycoheterotrophs in particular (Kinoshita et al. 2016) in unclear. The relationship between fungus and orchid is certainly not one-on-one (e.g. Martos et al. 2012: identification method important; Leake & Cameron 2012; Jacquemyn et al. 2013) and can even seem pretty random, at least in the ECM pezizalean associates (Tuber: ascomycetes) of Epipactis studied by Tesitelova et al. (2012). Individual North American clades in the mycoheterotroph Corallorhiza striata complex (Epidendroideae-Maxillarieae) are associated with different sets of the fungus Tomentella (Thelephoraceae: Barrett et al. 2010), and Bidartondo et al. (2004) discussed potential host specifity in several European orchids. Roche et al. (2010) studied the specificity of the Tulasnella-Chiloglottis association (see also Otero et al. 2011: Pterostylinae). Differentiation of fungal communities on different species of orchids may contribute to niche partitioning (McCormick & Jacquemyn 2013; Jacquemyn et al. 2013 and references). Nurfadilah et al. (2013) found that fungi varied in their ability to utilize nutrients in phosphorus-poor West Australian soils, suggesting that this might help explain the commonness of different species of orchids there, however, Davis et al. (2015) thought that specificity of fungus:orchid relationships was unlikely to explain the endemism of southern Australian orchids, rather, pollination by sexual deception and specific edaphic requirements might be a better explanation. And if the estimate by van der Heijden et al. (2015a) that around 25,000 species of fungi are associated with orchids is confirmed, this opens up all sorts of evolutionary possibilities...

The Epiphytic Habitat.

About 70% of Orchidaceae, some 18,850 species, are epiphytes, and they make up ca 70% of all epiphytic flowering plants (Benzing 1983; Zotz 2013). Epiphytes are particularly common in Epidendroideae, although not in Neottieae and some other basal clades (Freudenstein & Chase 2015). Chomicki et al. (2014c) estimated that the epiphytic habit had been acquired four to seven times and subsequently been lost rather more often, although details of the evolution of this trait are unclear. Diversification in the speciose crown/advanced/upper Epidedendroideae, with seven or eight tribes and largely epiphytic, began 37.9-30.8 m.y.a. (Gravendeel et al. 2004; Givnish et al. 2015; see also Freudenstein & Chase 2015). Speciation may increase in these clades, e.g. in Epidendroideae-Malaxidae-Dendrobiinae, partly because of the adoption of the epiphytic habit and movement into montane areas, and apomorphies deeper in Orchidaceae, while having no obvious immediate effect on diversification, also combined to affect diversification at these higher levels (Givnish et al. 2015: see also below). On the other hand, in Epidendreae-Calypsoinae, but largely terrestrial, a reversal), there is a decrease in the rate of speciation (Givnish et al. 2015, see also 2016a).

Nyffeler and Eggli (2010b) estimate that some 50+ genera and 2,200 species, especially epiphytic species - or perhaps double that number - are succulent. They have thickened leaves and quite often a thickened stem, whether corm or pseudobulb, although this feature is also quite often absent (Feudenstein & Chase (2015). In the epiphytic habitat orchids have to deal with periodic drought and lack of nutrients (Gravendeel et al. 2004, see also Motomura et al. 2008), rather like in the dry terrestrial habitats where succulence is also common (see also Figueroa et al. 2008); terrestrial orchids have thinner leaves. Epiphytic orchids often have very thick roots with very well developed velamen and exodermis with tilosomes on top of the living passage cells, pneumathodes are sometimes present, and any root hairs are primarily for anchoring the plant to the twig (e.g. von Guttenberg 1968; Pridgeon 1987: comprehensive; see Siegel 2015 for a readable account). Perhaps 9,700 species of Epidendroideae have crassulacean acid metabolism (CAM) photosynthesis (very approximate estimate based on Winter & Smith 1996b); variants of CAM photosynthesis such as CAM-cycling are also common (see Cameron et al. 2008 for Oncidiinae; Winter et al. 2015). (The actual number of taxa involved is unclear. In a survey of 1,002 Costa Rican orchids, only some 10% of Vanilloideae and Epidendroideae were found to show signs of strong CAM, perhaps 30% more had weak CAM; CAM was not found in Orchidoideae and Cypripedioideae - Silvera et al. 2010a.) CAM may have evolved four times or so in the family (Givnish et al. 2015). Cauline pseudobulbs, common in epiphytic orchids, may carry out CAM even although they lack stomata. CAM occurs in Bulbophyllum minutissimum, however, since the pseudobulb of Bulbophyllum is a modified leaf, even if lacks a blade, one presumes there are stomata (Kerbauy et al. 2012 and references). CAM has evolved perhaps ten times in Orchidaceae, it has also reversed to C3 photosynthesis, and there are intermediates. The photosynthetic pathway in root and leaf may be different, the former being C3 while the latter is CAM (Martin et al. 2010). Adoption of CAM is predominantly by epiphytic Epidendroideae growing at low altitudes and drier conditions (Silvera et al. 2009; Kerbauy et al. 2012) and has been linked to the Caenozoic radiation of that subfamily (Silvera et al. 2009). CAM photosynthesis has also evolved perhaps four times (and reversed once) in terrestrial Eulophiinae, also Epidendroideae (Bone et al. 2015b). In the Madagascan Eulophiinae adoption of CAM may have allowed the orchids to move into drier habitats (Bone et al. 2015b). Gene duplication has been implicated in the functional diversification of genes like phosphoenolcarboxylase involved in CAM photosynthesis (Silvera et al. 2014), although Deng et al. (2015) that the number of duplicates may be irrelevant as regards photosynthesis type.

Another problem faced by epiphytic plants is damage to tissues caused by UV-B radiation. Twig epiphytes in particular, concentrated in a clade of the New World Epidendroideae-Cymbidieae-Oncidiinae, face such problems. They grow on twigs less than 2.5 cm in diameter and in very exposed and high light conditions. Recent work suggests that chalcone synthase genes can be induced by UV-B light in the root tips of epiphytic orchids, and as a result UV-B-absorbing flavanoids are synthesised (Chomicki et al. 2014c: for sunlight and epiphytism, see also Bromeliaceae). A leafless orchid was included in this study and it showed behaviour similar to that of the two leafy epiphytic taxa examined.

Mycorrhizal associations are usually less common in epiphytes (e.g. Janos 1993; Desirò et al. 2013). However, the basidiomycetes Sebacinales group B and Tulasnellales (= Cantharellales) are ECM associates of neotropical epiphytic orchids, species of Tulasnellaceae, at least, colonizing more than one species of orchid (Kottke et al. 2008; see also Martos et al. 2012; Gowland et al. 2013), while in montane South America Sebacinales are in clades close to but separate from clades that form distinctive modified ericoid mycorrhizae in Ericaceae growing in the same habitats (Setaro et al. 2013). Basidiomycete fungi are to be found in the photosynthetic roots of the leafless epiphyte Dendrophylax lindenii (Chomicki et al. 2014b). In addition to the implications such mycorrhizal associations have for the nutrition of the epiphytic orchid, there may also be associations between aerial roots of the orchids and nitrogen-fixing cyanobacteria and interactions with other bacteria from the rhizosphere (Teixeira da Silva et al. 2015: focus on Dendrobium).

The leaves of some epiphytic Epidendroideae-Vandeae are very small and not photosynthetic and/or soon deciduous, and the vegetative plant consists largely of photosynthetic roots. These roots may be stout (ca 5 mm across) and terete, as in Dendrophylax, while the roots of the aptly named Taeniophyllum are distinctively flattened (e.g. Carlsward et al. 2006b). There are over 200 species of leafless Epidendroideae, all epiphytes, with an estimated 20 or morwe independent losses of leaves (Freudenstein 2012). How carbon dioxide and water flux are controlled in leafless epiphytes is unclear, especially because there are no stomata in the roots, although the aeration units may be stomata analogues (Benzing et al. 1983; Cockburn et al. 1985). Roots of leafless orchids like Campylocentrum tyrridion, which lack stomata, also carry out CAM (Kerbauy et al. 2012; Winter et al. 2015). Photosynthesis in orchid roots is poorly understood.

Twig epiphytes in Oncidiinae are particularly distinctive. They grow on twigs less than 2.5 cm in diameter and their seed coats have little grapnels, perhaps aiding in their attachment to the twigs (Chase & Pippen 1988). The plants are very small and may mature within a year (Chase 1987; Chase and Palmer 1997; Neubig et al. 2012a); indeed, many of these epiphytes are exposed to light immediately on germination, rather than starting off with a slow-growing subterranean mycotrophic phase (Leake & Cameron 2012). Their leaves are isobifacial or otherwise strongly laterally flattened and are arranged like a small fan or in two ranks (the psygmoid habit) and the plants have no pseudobulbs. All in all, they look like very young plants of other Oncidiinae and are more or less paedomorphic (Chase 1987; Neubig et al. 2012a for references; Chase et al. 2005 for genome size).

There have been some reversals from epiphytism to the terrestrial habit in Epidendroideae. These include Bletia and its relatives, one of which, Hexalectris is mycoheterotrophic and grows in quite dry conditions in North America (Sosa et al. 2016). There has also been a reversal to the terrestrial habit in Malaxidae (Cameron 2005).

For myrmecophytism in Myrmecophila (Epidendroideae), which grows in dry and open environments, even sand dunes, see Rico-Gray et al. (1989) and Pridgeon et al. 2005).

Pollination Biology & Seed Dispersal.

Pollination Biology.

Orchid flowers may be notably long-lived (months), although some last only for a single day. Flowers are commonly resupinate, the ovary being twisted about 180°, the labellum ending up in the abaxial position (Ernst & Arditti 1994; Yam et al. 2009 for reviews). However, the amount of resupination often varies within a plant when the inflorescence is arching; all flowers of the inflorescence are oriented so that their labellum is in the same position with respect to gravity, with the ovary sometimes being twisted 360° (as in Angraecum, etc.) or not at all. Catasetum has resupinate staminate flowers, but the carpellate flowers are not resupinate (see below). Fischer et al. (2007) discuss the variety of ways - of which twisting of the pedicel is but one of the mechanisms involved - that flowers in the speciose Bulbophyllum present themselves in the Malagasy region. In genera like Calopogon the flowers are never resupinate, and all flowers on the erect inflorescence show "normal" monocot orientation, the labellum being adaxial.

The most conspicuous element of the flower is often the labellum, a member of the inner whorl of tepals, which shows a truly remarkable diversity of form and colour (Rudall & Bateman 2002; see also 2004); duplication of genes may be involved (Mondragón-Palomino & Theißen 2008). The column is formed from the androecium and stigma/style, and there is generally only a single stamen with the pollen grains variously aggregated into pollinia. The spatial relationships of the labellum and column in particular force the pollinator to approach the flower in a particular way, and in general, pollinaria are usually very precisely placed on the pollinator, closely related orchid species differing in exactly where their pollinaria are placed (e.g. Maad & Nilsson 2004). After the pollinarium is attached to the pollinator, the pollinia may move, so bringing them into the proper position for pollination; for pollinia, pollinaria, and pollen deposition - not always in one go even when there are pollinia, e.g. Listera (= Neottia, Epidendroideae), see Rasmussen (1982), Freudenstein and Rasmussen (1996, 1997), Nazarov and Gerlach (1997), Johnson and Edwards (2000), Pacini and Hesse (2002), Freudenstein et al. (2002), Harder and Johnson (2008), Selbyana 29: 1-86. 2008, and so on. The plesiomorphic condition for Orchidaceae is to have elastoviscin (quite different from the viscin threads of, say, Onagraceae) associated with the pollen grains. It is very similar to pollenkitt, although tapetal plastids seem not to be involved, and makes up the stipe of the pollinaria in some orchids, or can be entirely lost (Still & Wolter 1986).

A final distinctive feature of many orchid flowers is that the ovules are usually not fully developed - and may not even be recognizable - at anthesis, and fertilization is then delayed relative to pollination, as in Cypripedium. The time between pollination and fertilization ranges from four days to ten months (in Vanda), the normal time being one week to six months (Wirth & Withner 1959, Yeung & Law 1997; also Sogo & Tobe 2005, 2006d for references: ?Apostasioideae). Even after fertilization, it may be a month before embryo development begins, as in Sarcanthinae (Wirth & Withner 1959 for references).

Note that selfing in orchids may be quite common (Gamisch et al. 2014 for a review). The bee-mimic Ophrys apifera may self-pollinate if not visited by bees; there the pollinia curve downwards and meet the stigma. There are other selfing mechanisms, too, as in Paphiopedium parishii where the contents of the anther liquefy and slop on to the stigma (L.-J. Chen et al. 2013). In Madagascan Bulbophyllum selfing varies infraspecifically and is associated with the loss of the rostellum, as it often is elsewhere in the family (Gamisch et al. 2014; see also e.g. Peter & Johnson 2009). For selfing in Angraecum from the Mascarenes, an area where there are no sphingid pollinators, see Michenau et al. (2014: many other orchids there self, see references).

In the following brief discussion on orchid pollination, I emphasize first rewards, then the pollinator, with some other issues mentioned at the end. For pollination, see also van der Pijl and Dodson (1966).

Rewards - or Lack Thereof.

The plesiomorphic condition for the family may be to lack nectar (Jersáková et al. 2006; for rewardless flowers in general, see Renner 2006a); all told, perhaps 8,000 or more species of orchids lack nectar (but some have other rewards, and species with rewards may be more common than thought - Karremans et al. 2015). Apostasioideae have pollen as a reward for pollinators (Kocyan & Endress 2001), but deception may well have occurred in the common ancestor of the rest of the family (Weston et al. 2014; Givnish et al. 2015). Cozzolino and Widmer (2005; see also Schiestl 2005) suggested that orchid diversification is associated with the mimicry/deceptive pollination mechanisms that are so prevalent in the family; about one third of the species - estimates range from 6,500 to 10,000 - are pollinated in this way (Safni 1984; Ackerman 1986; Schiestl 2005, 2010 for reviews, the latter brief; Schlüter & Schiestl 2008: molecular mechanisms; Peakall 2009: deceit and speciation; Schaefer & Ruxton 2010: exploitation of perceptual biases of the pollinator by the plant; Gaskett 2011: the pollinator's point of view in sexual deception; Xu et al. 2012; Pinheiro & Cozzolino 2013: deceit in Epidendrum). Deceit comes in various guises, from sexual deceit, where the orchid mimics a female insect and pollen exchange occurs during pseudocopulation (e.g. Ophrys below), to domicile deceit, as in species of Serapias (Orchideae: Bellusci et al. 2008 for a phylogeny) and Cypripedium (Cypripedoideae: Pemberton 2013) that attract pollinators by mimicking a nest hole, and more generally, appearing to have rewards, whether a fungal body or carrion where insects can lay eggs, but in fact lacking them (Kagawa & Takimoto 2015 and references). There are more complex situations where flies (Drosophila in this case) are attracted to flowers by aggregation pheromones, but there is nectar reward and the flies may copulate when on the flower (Karremans et al. 2015). See also the section on pollinators below, especially dipterans.

Flowers of the European Ophrys (Orchidoideae-Orchideae) are well known for deceit pollination, their labellum mimicking female bees and wasps (e.g. Kullenberg 1961; Paulus 2006). They also produce chemicals that are very similar to insect pheromones; alkenes (hydrocarbons with at least one double bond) are part of the chemical component of this mimicry (e.g. Stökl et al. 2009; Ayasse et al. 2011; Xu et al. 2012). Morphology and scent together enable the Ophrys flower to mimic female insects (Cortis et al. 2009 and references), pollination occurring as male bees and wasps in particular attempt to copulate with the flowers (Kullenberg 1961; Kullenberg et al. 1984 and references). Barriers to crossing - floral form and scent again - act before pollination, and no deleterious effects of hybridization, which occurs in the wild, have been noted (Xu et al. 2011). Scent chemicals are common in related genera as well (Schiestl & Cozzolino 2008), and Ophrys is part of a larger clade in which food deception seems to be the basic condition (Inda et al. 2012). However, there is currently much discussion about species limits in Ophrys, with estimates of species numbers ranging from 16 to 252 (Bateman et al. 2006a, 2011a; Devey et al. 2008; Bradshaw et al. 2010; Vereecken et al. 2011; see Delforge 2006 and Alibertis 2015 [half the book!] for photographs of the species/"species"). Paulus (2006: p. 315) thought that "species formation in Ophrys always proceeds with the aquisition of a new species of pollinating males", and species that had different pollinators might show "genic rather than genome-wide differences", speciation had barely begun (Sedeek et al. 2014: p. 6202); see also floral scent bouquets in these orchids and species limits (Joffard et al. 2016). Rapid diversification in the Pleistocene accompanied shifts to different pollinators, from wasps to apid or andrenid bees (Breitkopf et al. 2015).

Around 100 species of Australian Caladenia (Orchidoideae-Diuridae) are pollinated by male thynnine wasps (Phillips et al. 2009, other articles in Australian J. Bot. 57(4). 2009; see also Brown & Brockman 2015). In another Australian genus, Chiloglottis (also Diuridae), where scent also plays a role in maintaing reproductive isolation (Peakall & Whitehead 2013), there is a fair degree of congruence between the phylogenies of the orchids and the deceived wasps (Mant et al. 2002, 2005; see also Weston et al. 2011; Miller & Clements 2014). In both cases understanding species limits is critical; there seem to be a number of cryptic species, hybridization occurs, etc. (see also Jones et al. 2001; Griffiths et al. 2011). In such sexually-deceptive orchids both morphological and genetic differences between species or even genera are slight (Schiesl 2005 and references; Mant et al. 2005; see also below) and post-pollination barriers may be nonexistent (Whitehead & Peakall 2014).

Chemical signalling between plants and insects involved in pollination occurs in many situations, not only enhancing floral mimicry in pseudocopulation. Thus wasps may be attracted to orchid flowers that produce chemicals similar to those produced by damaged plant tissue - the wasps visit the flower expecting to find caterpillars, but pollination occurs instead. Similarly, Dendrobium sinense, pollinated by a hornet, has a floral bouquet that includes the same chemicals as in the alarm pheromones of Apis, which the hornet commonly catches (Brodmann et al. 2009). The volatile emissions of some orchids produce signal various kinds of decaying tissue, so attracting insects that pollinate the flowers (see Jürgens et al. 2013 for the syndromes).

Other kinds of food deceit are quite common, as with pollen mimicry in Vanilloideae-Pogonieae where it characterises a clade that includes temperate species; pollen is apparently available for removal (Pansarin et al. 2012). Nectar deceit is also common in Caladenia (Phillips et al. 2009). A number of species of Epidendroideae-Oncidiinae have flowers like those of oil-producing Malpighiaceae, q.v.. They have radiating, clawed, yellow or purple "petals" that are similar in both shape and in colour, bee-UV-green, to flowers of Malpighiaceae, and they may be part of a Batesian mimicry system, both groups being visited by bees like Centris. The orchids often have no reward for the bee (Neubig et al. 2012a; esp. Papadopulos et al. 2013; see also below). The mimicry unit of the orchid is formed largely by the labellum, the column being equivalent to the banner petal of a malpighiaceous flower. M. P. Powell (in Neubig et al. 2012a) has estimated that such mimicry may have evolved at least 14 times within Oncidiinae, indeed, it may be both lost and regained (Papadopulos et al. 2013). Some Oncidiinae mimic Calceolaria, another oil flower (Neubig et al. 2012a), and floral mimicry is also known from the largely Australian Thelymitra which has sub-polysymmetric flowers (Edens-Meier & Bernhardt 2014a). Attractive orchid flowers that lack any rewards may have polymorphic flowers, if the pollinator is not that good at discriminating colours (and a rather slow learner), or more continuous variation, if the pollinator is better at distinguishing colours (Kagawa & Takimoto 2015).

Flowers of many orchids do have rewards for the pollinator, and such flowers have frequently been derived from flower lacking rewards (Cozzolino et al. 2001; Cozzolino & Widmer 2005; Smithson 2009; Pansarin et al. 2012; Johnson 2013). Thus in the speciose African Disa (Orchidoideae), there have been several transitions from deceit to nectar rewards, and loss of nectar, and independent gains and losses of spurs - all without having much of an effect on diversification rates (Johnson et al. 2003). The production of rewards may also be derived in Vanilloideae-Pogonieae (c.f. Pansarin et al. 2012).

Pollen alone is collected from flowers of Apostasioideae, and even from some Vanilloideae (Pansarin et al. 2012). Nectar flowers are quite common (Bernadello et al. 2007 and references). Nectar is quite a common reward, and although Orchidaceae never have septal nectaries, nectar spurs are scattered in the family. For spurs, nectariferous and otherwise, in Orchidoideae-Orchidinae, including Habenaria, see Bell et al. (2009); the flowers of Satyrium are not resupinate and have twin nectar spurs (Johnson et al. 2011a). For nectar spurs, which develop from the adaxial sepal, in the largely Australian Diurideae, see the summary in Weston et al. (2011, 2014), and there are also various kinds of mimicry, and nectar production - sometimes from the labellum - has evolved, and then perhaps been lost many times. Spurs are common in Vandeae (Angraecum Angraecinae, see above, Aeridinae, see Topik et al. (2005). Tissue on the tepals may also produce nectar (Davies et al. 2005; Hobbhahn et al. 2013). Hobbhahn et al. (2013) discuss the evolution of nectaries of various types (a secretory nectariferous epidermis is here descibed as being "recapitulatory") in Disa, which happened some eight times there alone.

Resins and oils are also quite common rewards; for a summary of oil flowers in Orchidaceae, which have evolved probably at least a dozen times, eight times in Maxillarieae alone, see Renner and Schaefer (2010). In a number of species of Maxillaria hairs on the labellum contain protein and perhaps also starch and function as pseudopollen, so rewarding the pollinator (Davies et al. 2000; Davies 2009). Resins as a reward have evolved several times in Maxillaria and its relatives, and flowers of some species mimic the presence of resin rewards (Whitten et al. 2007; Davies & Stpiczynska 2012). Orchids with oil as a reward may show convergence with the flowers of other oil-pollinated plants. Some 70 species of Oncidiinae have elaiophores, often on the labellum; these may be epithelial or tufts of secretory hairs (Blanco et al. 2013; Davies et al. 2014 and references) and be visually similar to elaiophores on the calyx of Malpighiaceae, or the flower as a whole may be like those of Malpighiaceae. The distinctive oil secreted is very similar to that produced in the flowers of Malpighiaceae (see above; Reis et al. 2007 and references), and there may be some kind of Müllerian mimicry system here (Papadopulos et al. 2013), but such systems are difficult to categorise (see also Policha et al. 2014). Pollination of some South African Orchidoideae-Coryciinae (e.g. Disperis) is by oil-collecting bees; the flowers have paired, pouch- or spur-like structures like those of another local oil plant, Diascia (Scrophulariaceae: Pauw 2006). The South African Huttonaea, perhaps immediately unrelated, also has oil flowers (Steiner 2010); Steiner et al. (2011) analyzed scent composition of many southern African oil-secreting Diseae. Fragrances are commonly collected by male orchid bees (see below). See also Chase et al. (2009) and Steiner (2010) for oil flowers.


Turning now to different pollinator groups, fly pollination is common (Christensen 1994; Siegel 2016 for a readable summary), especially in Epidendroideae. Thus the very speciose and largely Old World Bulbophyllum often has dark, purplish-coloured flowers, the labellum is mobile, and there may be dangling structures (hairs of various kinds, labellum tips), and it attracts a variety of flies. A number of taxa have sweet, fruity scents and lighter-coloured flowers and are pollinated by fruit flies - which may also be commercially important pests (Tan 2008 and references, see also Texeira et al. 2004; Fischer et al. 2007 for resupination there). In some African species, Stpiczynska et al. (2015 and references) found species with scented flowers and nectar (secreted by the labellum), or lipids as a reward, and the labellar tissue might be aerenchymatous, presumably increasing its mobility. Some species have flowers with a carrion scent suggesting pollination by necrophagous insects, as Siegel (2016: p. 87) noted of the flowers of B. fletcherianum, they smell "like a herd of dead elephants". However, as with other megagenera, little is really known about pollinators and floral rewards here, and the floral diversity of the genus beggars description (see e.g. the illustrations in Vermuelen et al. 2015). In the large New World Lepanthes, pollination during pseudocopulation with fungus gnats (dipterans, often Sciaridae) has been reported (Blanco & Barboza 2005). How this system might function is unclear since there is no obvious connection between the morphology of the orchid flower and that of the fungus gnat (Singer 2011). Fungus-visiting drosophilids pollinate Dracula, which can have a labellum that looks (and smells) very much like a fungus with gills, as well as a distinctively patterned "calyx", and other flies are also involved (Policha 2014; Policha et al. 2014, esp. 2016). Stimulation of the labellum by ?flies visiting the flowers of Porroglossum causes it to snap shut, imprisoning the insect against the column whence they remove the pollinaria, and the trap reopens after some minutes (Pridgeon et al. 2005; McDaniel & Cameron 2016). Indeed, a variety of dipteran groups pollinate orchids, sometimes nectar is a reward, or the orchid simulates decaying material or a fungus (sapro- or mycomyophily), and these modes of pollination are likely to predominate in the some 4,000+ species of Epidendroideae-Pleurothallidinae, to which Lepanthes and Dracula belong (Pridgeon et al. 2005 and references; Karremans et al. 2016). Here self incompatability tends to be developed, as in some other Epidendroideae (Borba et al. 2011; Duque-Buitrago et al. 2014; Karremans et al. 2015). Pollination by Drosophila and Scatophaga is also known in Cypripedium (Li et al. 2012; see Edens-Meier et al. 2014 for Cypripedoideae in general), while carrion flies pollinate Satyrium pumilum (Orchidoideae-Diseae: van der Niet et al. 2011).

Moth, butterfly, and even bird pollination are also well known in the family. Angraecum sesquipedale (Epidendroideae-Vandeae), from Madagascar, is a classic example of moth pollination. There the spur is 30-45 cm long, and the pollinator for long remained unknown, although Darwin (1862) suggested that some moth with a proboscis that long would be found. Indeed, Xanthopus morgani praedicta, with a proboscis length of about 25 cm, was subsequently discovered (Nilsson et al. 1987; Nilsson 1988: Wasserthal 1997; Arditti et al. 2012); see Micheneau et al. (2010) for pollination in the over 200 species of angraecoid orchids. For the great floral and pollinator diversification in some genera of Orchidoideae-Orchidinae, including Disa, see Johnson et al. (1998, 2013) and Bytebier et al. (2007).

It has been estimated that perhaps 60% of Orchidaceae are pollinated by bees (Schoonhoven et al. 2005), whether deceived or not. Williams (1982) discussed the general importance of male euglossine bees in particular in the pollination of neotropical Epidendroideae (see also Roubik 1988, 2014). Male bees pollinate the flower as they collect fragrances that they store in their hind tibial pockets, these fragrances perhaps being involved in pre-mating isolation in the bees (Zimmermann et al. 2009). There are some 190 species of orchid bees and they pollinate perhaps up to 25% of tropical American Orchidaceae, hence their common name, orchid bees. Some 700 species of orchids have fragrances that attract male bees, an estimated 85% of all plants with such fragrances (Ramírez 2009); another estimate is that perhaps 2,000 species of Epidendroideae (i.e. almost all Stanhopeinae, Zygopetalinae and Cataseteinae) are visited by male euglossines for fragrances (see e.g. Williams 1982; numbers from Pridgeon et al. 2009). Euglossine pollination in general is especially common in orchids growing at lower altitudes, and anywhere from 900-2,000 species may be so pollinated (Cameron 2004 and references; Zimmermann et al. 2009; Ramírez et al. 2011 - Photo: bee pollinators). For further discussion about euglossine pollination, see Clade Asymmetries.

How Catasetinae, Catasetum in particular, are pollinated by male euglossine bees is well known (Darwin 1862; Chase & Hills 1992 and Pérez-Escobar et al. 2015 for a phylogeny; Gerlach 2013). Catasetum has remarkable flowers, even for an orchid. Not only may resupination differ between staminate (resupinate) and carpellate (non-resupinate) flowers, but there are many other striking differences, especially in labellum morphology, between the two; indeed, staminate and carpellate specimens were once put in separate genera, Myanthus and Monachanthus respectively. The attachment of the pollinaria on the bees is by a trigger-activated explosive mechanism (Nicholson et al. 2008). The insect is startled, and Romero and Nelson (1986) suggested that as a result the bees subsequently avoided staminate flowers, hence the very different morphologies of the carpellate flowers, which, however, are more similar between the species: "The battered pollinator will remember the negative experience with the staminate flower" (Gerlach 2012: p. 39). A final wrinkle is that the kind of flower produced is determined, at least in part, simply by light; bright light tends to favour the production of carpellate flowers (Gregg 1975); Pérez-Escobar et al. (2015) found that environmental sez determination had evolved three times here, with 164 species being involved (Catasetum, Cynoches, some Mormodes).

Although euglossine bees are effective pollinators, the relationships between orchids and bees are non-specific on both sides, particularly on the side of the bee (Ackerman 1983; Cameron 2004; Ackerman & Roubik 2012), although Stebbins (1970) thought that both bee and orchid speciated extensively. Importantly, crown-group euglossines can be dated to 42-27 m.y.a., with especially rapid diversification 20-15 m.y.a. (Ramírez et al. 2010) or (35-)28(-21) m.y.a. (Cardinal & Danforth 2011). (Stem-group euglossines are Cretaceous in age - e.g. Grimaldi & Engler 2005.) The orchids these bees pollinate speciated abou 12 m.y. later, (31-)27-18(-14) m.y.a (Ramírez et al. 2011) or 22-16 m.y.a. (Givnish et al. 2015: two origins), the estimates being from Catasetinae and Zygopetalinae plus Stanhopeinae, immediately unrelated clades. Most of the compounds that the bees pick up from the orchids are found elsewhere, and many other fragrances are acquired from other sources. Closely related and sympatric species of Euglossa did show greater disparity in the fragrances they preferred than might be expected, but overall, the most dominant compounds in the fragrances were highly homoplasious (Zimmermann et al. 2009).


The connection between the orchid-pollinator relationship and orchid diversification remains a matter of active discussion. Tremblay et al. (2005) reviewed the evolutionary consequences of the diversity of the pollination mechanisms of Orchidaceae and the remarkable variation shown by their flowers. Orchid diversification is often explained in terms of the close association between pollinators and individual species of orchids (?cospecation, ?coevolution), and pollination relationships are usually thought of as being very precise. Reproduction in orchids may often be pollinator-limited (Tremblay et al. 2005), with few flowers on an inflorescence producing seeds, however, the production of huge numbers of seeds by each fruit may compensate for this - as Pérez-Hérnandez et al. (2011) noted, orchids "specialize in chance". Interestingly, nectarless orchids have a lower reproductive success that orchids that have nectar as a reward (Kindlemann et al. 2007: sample size small, latitude unimportant), and reproductive success of tropical orchids may be lower than that of their temperate relatives, perhaps because it is more difficult for the pollinator to find the orchid in diverse tropical vegetation (Kindlemann et al. 2006); these patterns will interact with factors like pollinator specificity, etc..

Pollinator specificy in orchids can be overemphasized. A single species of Epipactis may be visited by over 100 species of pollinators (Tremblay 1992), while in another study, pollinator specificity in orchids, although greater than that in Ranunculaceae (but that hardly says much), was less than that in Polemoniaceae (Waser et al. 1996). Some orchids may be exquisitely adapted to individual pollinators whose sensory biases they may exploit (Schiestl 2010; Ramírez et al. 2011), but even here individual species of orchid bees, for example, may pollinate several species of orchids (Williams 1982), plant-pollinator relationships being highly nested; furthermore, few of the fragrances sought by male bees are unique to the orchids (Ramírez et al. 2011). Indeed, plant-pollinator specificity in euglossine orchid bees is lowest (from the bee's point of view) when a bee species is common and lowest (from the plant's point of view) when its flowering season is long, and seems to have little to do with in some way reducing extinction risk as by reducing dependence on unreliable pollinators - specificity is more apparent than real and is in part a matter of sampling (Ackerman & Roubik 2012).

Given the timing of evolution of orchids and bees, and the relative dependency relationships of the two, simple insect-orchid co-speciation is unlikely to be an important explanation for orchid diversification. Recent work suggests very strongly that strict co-speciation is unlikely (e.g. Williams 1982; Szentesi 2002; Jersáková et al. 2006; Ramírez et al. 2011). That the generation of diversity by floral specialization is relatively uncommon in flowering plants in general, although perhaps occurring in orchids (Armbruster & Muchhala 2009) is not inconsistent with this argument. Furthermore, factors other than floral variation may have contributed to orchid diversification - see also "Vegetative Variation" below and "Ecology & Physiology" above.

Recent studies suggest that when pollinators visit orchid flowers in the course of deceptive pollination or to pick up scent rewards - specialized pollination mechanisms - pollinator specificity is greater and species richness is greater than when pollinators visit for nectar (Schiestl & Schlüter 2009; Xu et al. 2011; Schiestl 2012: sister-group comparisons; see also Dressler 1968; Scopece et al. 2010a for pollination efficiency). Thus deceit pollination may under certain situations increase outcrossing and speciation, the latter perhaps because of the specificity of the pheromones produced by the plants (Jersáková et al. 2006; see also Ledford 2007).

The presence of well-developed and effective premating barriers in Orchidaceae may have obviated any pressure for the selection of postmating barriers (e.g. Whitehead & Peakall 2014). As a result, artificial crosses are often easy to make (some 110,000 have been made), and hybrids may have three or more genera in their parentage, although how these will look when generic boundaries are redrawn is unclear. Thus many genera in Laeliinae can be crossed artificially (van den Berg et al. 2000, 2009). In European orchids with generalized food-deceptive mating mechanisms, barriers to crossing may be postzygotic, whereas those that practice sexual deception have prezygotic reproductive barriers, and introgression is more likely in this latter situation (Cozzolino & Scopece 2008). Futhermore, Waterman et al. (2011) distinguish between speciation and coexistence in orchids, and note that shifts in details of pollination (placement of pollinaria, pollinating insect) occur with speciation, although associations with different fungi may promote the co-occurrence of immediately unrelated orchid species.

For summaries of pollination in Orchidaceae, see van der Cingel (1995, 2001), Endress (1994b), Biol. J. Linnean Soc. 173: 713-773. 2013, Pridgeon et al. (1999, 2001b, 2003, 2005, 2009, 2014), etc. - and of course the classic study by Darwin (1862a) is still worth reading (see also Yam et al. 2009; Edens-Meier & Bernhardt 2014b). For a general discussion on floral evolution in the family, with an emphasis on terata and homeosis s.l., see Rudall and Bateman (2002); Rudall and Bateman (2004: outgroup a Hypoxis-type flowers, but this is of no consequence) emphasize the various processes involved.

Seed Dispersal.

The minute dust seeds of most orchids are a distinctive feature of the family (e.g. Moles et al. 2005a). They are often produced in huge numbers, up to 4,000,000 seeds per fruit or 74,000,000 seeds per plant, and are as little as 150 µm long or less (Arditti & Ghani 2000; Yam et al. 2009). Orchidaceae have particularly small seeds when compared with their immediate relatives (Moles et al. 2005a), and they usually lack endosperm and the embryo is undifferentiated. Much of the seed, small as it is, is in fact empty space, and they are well suited for wind dispersal (Arditti & Ghani 2000); the trichomes on the endocarp quite commonly found in Orchidaceae may function as elaters aiding in seed dispersal (Kodahl et al. 2015). Although Arditti (1967) did suggest that a few species had recognizable cotyledons, the species mentioned are not basal in the tree. The subterrananean mycoheterotroph Rhizanthella has baccate fruits with large, crustose seeds (Weston et al. 2011). In Vanilla imperialis a white foamy substance exudes from the fruit, carrying the seeds along with it (Kodahl et al. 2015 - note the extensive variation in seed morphology in Vanilloideae), indeed, Rodolphe et al. (2011) suggest that seeds in Vanilla may sometimes be dispersed by euglossine bees.

Plant-Animal Interactions. Orchidaceae are not often eaten by caterpillars (Janz & Nylin 1998) or by insect herbivores in general, although Riodininae-Riodininae larvae may be found on them (Hall 2003 and references).

Bacterial/Fungal Associations. Orchids characteristically have a very close association between basidiomycete and some ascomycete fungi. Rhizoctonia (= Ceratobasidium) is a common anamorph or form genus that encompasses a multitude of sins (Dearnalay et al. 2012) - Russulaceae, Tuber, and Sebacinales-B (found with autotrophic orchids), in the same clade but in different subclades, from Sebacinales-B found on Ericaceae (Setaro et al. 2012, 2013) and Sebacinales-A (with mixotrophic and mycoheterotrophic orchids) are all involved. The commonest families are Tulasnellaceae (perhaps the most important group - Martos et al. 2012), Ceratobasidiaceae and Sebacinaceae (see Currah et al. 1997 and Yukawa et al. 2009 for lists of fungi; Otero et al. 2002; Roy & Selosse 2009; Weiß et al. 2009), but some neotropical Epidendroideae have Atractiellomycetes (in the same clade as Puccinia) as mycobionts (Kottke et al. 2010). The fungi associated with the plant as it germinates may be quite different from those associated with the adult plant (Hashimoto et al. 2012 and references; Rasmussen et al. 2015; Y.-I. Lee et al. 2015). Despite the wide distribution of some of their fungal associates, orchid species may be narrowly distributed (Davis et al. 2015: Sebacina the fungus). Overall, orchid fungal networks are not nested, that is, specialist fungi, forming associations with only a few species of orchids, are often not also found on generalist plants growing in the same area that are associated with fungi also found on other plants; in this they are like ectomycorrhizal are ericoid mycorrhizal associations (Toju et al. 2016 and references).

Although Rinaldi et al. (2008) thought that only 10 species of fungi might be involved in fungus:orchid associations, the number is far greater, even on a single species and in relatively small areas (e.g. Martos et al. 2012; Jacquemyn et al. 2013), while van der Heijden et al. (2015a) estimated that about 25,000 species of basidiomycetes are involved, as many as in the mycorrhizal associations of all other embryophytes combined. Martos et al. (2012) discussed the literature on the phylogenetic signal of orchid and fungus.

Yukawa et al. (2009) suggested that the basidiomycete Cantherellales may have been the fungus group first associated with Orchidaceae. At least some orchid fungi are probably saprophytes living on decaying plant material that can also form close relationships with orchids (Ogura-Tsujita et al. 2009; Yukawa et al. 2009; Lee et al. 2015).

Recent work on orchids growing on Réunion suggests that the nature of the mycorrhizal network in epiphytic and terrestrial species differs, with only 10 of the 95 fungal species (taxonomic units) recorded found in species from both groups. Furthermore, most of the species, whether restricted to one of the groups or occuring in both, were found on only one or two of the orchid species (Martos et al. 2012). Differences between the species of fungi found in the two habitats, or in features of the orchids that affect colonization by the fungi, may both explain this striking pattern (Leake & Cameron 2012). Chomicki et al. (2014b) discussed the association of the root-photosynthetic epiphyte Dendrophylax (see below) with endomycorrhizal fungi.

For endophytic fungi, see Bayman and Otero (2006). Very little is known about them, and the one fungus may even be pathogen, endophyte, and mycorrhizal symbiont.

Vegetative Variation. Orchidaceae show considerable diversity in habit and other vegetative features despite their generally modest size. However, some Sobralieae are slender, cane-like plants up to about 10 m tall, while viny Vanilloideae, even including the mycoheterotrophic Galeola, may be several metres long. The geophytic habit is quite common in Orchidoideae in particular. Stems, leaves and even roots may be succulent (Nyffeler and Eggli 2010b; also Figueroa et al. 2008: see above). Leaves are variously arranged (but not opposite), and may be terete or isobifacial, while individual leaf blades of taxa like Bulbophyllum fletcherianum may be up to 2 m long, some 15 cm across and about 5 mm thick (B. minutissimum is 3-4 mm tall!). Tatarenko (2007) summarized the extensive vegetative variation of temperate orchids, i.e. especially Orchidoideae.

The roots of mature plants of "leafless" Epidendroideae-Vandeae and those of many other Epidendroideae appear to lack root hairs, although they may develop on the side of the root facing the substrate (von Guttenberg 1968; Pridgeon 1987). Bernal et al. ((2015) report distinctive spiral thickenings on root hairs of some Orchidoideae-Spiranthinae), the hairs being described as a continuation of the velamen, and they are interspersed among other root hairs - which also look rather distinctive. Rasmussen (1995) noted that in some ground-dwelling orchids the root apex might change directly into a shoot, or shoots might develop from roots, or new roots might grow down the middle of the rhizome.

Moreira and Isaias (2008) found that the terrestrial orchids they examined had thicker roots than did the epiphytic orchids, but the latter do often have very thick roots. In epiphytic orchids in particular a velamen, made up of dead cells with spiral thickenings on the cell walls, is well developed around the outside (von Guttenberg 1968; see below). Pneumathodes are common in Epidendroideae. Leafless Vandeae have aeration units, distinctive exodermal cells, a space beneath, and a pair of thin-walled cortical cells in their roots; such aeration units are also found in related leafy Vandeae (Benzing et al. 1983; Carlsward et al. 2006a, b). Roots of New World epiphytic Epidendroideae in particular have distinctive tilosomes, cells of the innermost layer of the velamen that are adjacent to the passage cells of the exodermis and that have complex often lignified excrescences developing from the wall (Pridgeon 1987; Pridgeon et al. 1983; Porembski & Barthlott 1988). However, such cells are also found in ground-dwelling Orchidoideae-Spiranthinae (Figueroa et al. 2008) and their exact function is unclear. Some epiphytic Epidendroideae lack much in the way of leaves, the roots, sometimes flattened, carrying out photosynthesis for the plant (see above).

The vernation of orchid leaves varies. The blade may be quite thin to very thick, bifacial, isobifacial or unifacial (terete), and the leaf base is sometimes massively swollen (Bulbophyllum). Leaves may be spirally arranged to 2-ranked, and are sometimes deciduous, being articulated with the sheathing base as is common in Epidendroideae. Some ground- and shade-dwelling species have distinctively-coloured and -patterned leaves - variegated, purple-mottles, two surfaces of different colours (e.g. Bone et al. 201b5: variegation = absence of chlorophyll?) - that makes them particularly attractive to horticulturists. Extrafloral nectaries are scattered, being found on the stems opposite the leaves in Vanilla, at the bases of the pedicels in Cymbidium, etc.

The End. We can now return to the question, Why are there so many orchids? Orchidaceae are distinctive in several ways, of which their flowers and fruits are just two. Vegetative and physiological variation, more or less associated with habit and habitat, is almost equally striking. Although no one feature of itself is likely to be responsible for orchid diversification, the main clades of the highly speciose and commonly epiphytic-CAM crown Epidendroideae, with eight or so tribes and around 19,560 species (figures from Pridgeon et al. 2005, 2009, 2014), i.e., about two thirds of the species in the family, may have diverged from each other only 37.9-30.8 m.y.a., diversification rates for the clade as a whole and even more so for some clades within it being notably high (Givnish et al. 2015, 2016a: c.f. stem age of subfamily!). A number of other features, most not closely associated with crown Epidendroideae, although pollination by orchid bees may be restricted to two clades in this group, may also have contributed to the increased diversification. Epidendroideae in particular are diverse in montane habitats in New Guinea, South America, etc., and the geography of such areas may also have facilitated speciation (Givnish et al. 2015). All this is against a background of festures like flowers with a column and labellum, and minute, endospermless seeds, which while common to the whole family and not immediate causes of orchid diversification, formed the substrate, as it were, for the subsequent radiation of the family (Givnish et al. 2015). Of course, the caveats mentioned above about thinking about orchid diversification without also thinking about the evolution of the whole [Asparagales + commelinid] clade apply, and overall Orchidaceae with their distinctive flowers show aimilar phylogenetic/diversity patterns as do angiosperms with their distinctive flowers.

Genes & Genomes. The rate of molecular evolution in the plastome is notably high in Orchidaceae when compared with other Asparagales (Barrett et al. 2015b).

There is much variation in chromosome number and size. Thus Apostasioideae, Epidendroideae and Orchidoideae have small chromosomes, while larger chromosomes occur in Cypripedioideae and Vanilloideae. Felix and Guerra (2010) survey chromosome number variation in Epidendroideae and I. de Oliveira et al. (2015) that in Pleurothallidinae; Epidendreae as a whole may be x = 20. For genome size, which varies 168-fold, see Leitch et al. (2009), Jersáková et al. (2013) and Yin et al. (2016).

The subterranean holomycotroph Rhizanthella (Orchidoideae-Diuridae) has a very small plastid genome, about 59,000 BP, but there is still a core group of functioning genes (Delannoy et al. 2011), and over two dozen functional gene were found in the still smaller genomes of Epipogium, to 19 kbp (E. roseum), the particular genes remaining functional depending on which essential genes had moved to the nucleus, etc. (Schelkunov et al. 2015). Barrett et al. (2014a, esp. b) discuss how the plastome has degraded in Corallorhiza. All members have at least some chlorophyll, but the amount of the plastome retained is about inversely proportional to how much photosynthesis going on in the plant.

MatK in Apostasioideae may be in transition from a possibly functional gene to a pseudogene; in other Orchidaceae examined (but the sampling is poor) it is a pseudogene (Kocyan et al. 2004).

Chemistry, Morphology, etc. Pyrrolizidine alkaloids are known from genera like Phalaenopsis and Pleurothallis (see also Nurhayati et al. 2009); for lignin with catechyl units, see F. Chen et al. (2012).

For the velamen and its systematic significance, see also Porembski and Barthlott (1988); there is some doubt as to whether or not Apostasioideae have a velamen; here I follow Pridgeon (1987). Furthermore, Porembski and Barthlott (1988) noted that all Apostasioideae, also a number of Orchidoideae, Cypripedioideae, etc., had a rhizodermis, but Pridgeon (1987) scored only the single Apostasioideae he examined and no other orchid as having a simple epidermis; one might have thought that a rhizodermis and a simple epidermis were the same thing... Orchidaceae are one of the few non-commelinid clades with SiO2 bodies (e.g. Prychid et al. 2003b), and these show some variation in form and are sometimes lost (Freudenstein & Rasmussen 1999). Paphiopedilum, but not other Cypripedioideae, lack chloroplasts in stomatal guard cells (D'Amelio & Zeiger 1988: other oddities in the family).

Cardoso-Gustavson et al. (2014) discuss the occurrence of often mucilage-secreting bicellular hairs ("colleters") in the flowers of Epidendroideae. They note that these may be on the outside of the flower, and suggest they may be connected with the extrafloral nectaries on the inflorescences of some Epidendroideae.

Monosymmetry of the flower in many, but not all orchids - and in Hypoxidaceae and Doryanthaceae - is evident even in the earliest primordia (Kurzweil & Kocyan 2002 and references). A few Orchidaceae have more or less polysymmetric flowers, and in Telipogon (Epidendroideae - Oncidiineae) a polysymmetric perianth becomes evident only late in development (Pabón-Mora & González 2008). Duttke et al. (2012) discuss the remarkable terata to be found in Neofinetia falcata (Vandeae: Aeridinae) that have been accumulated in Japan over the last 350 years. For floral development and the expression of B-, C- and D-class genes in particular in Dendrobium, see Y. Xu et al. (2006); genes of all three classes are expressed in the column. Hsu et al. (2015) suggest how labellum development might be controlled; there was gene duplication after divergence of the lipless Apostasioideae. Rudall et al. (2013b) attempt to work out what some of the parts of orchid flowers "are". They suggest connections between the auricles, which often have raphides, with inner whorl anthers of Apostasioideae, and they show that the bursicle, which had also been thought to be of staminodial origin, develops from lateral lobes of the median carpel. The labellum, which in its lobing they describe as being analogous to a compound leaf, has three traces - two come from the lateral sepals or perhaps originally from stamens of the outer whorl (Rudall et al. 2013b). The sequence of organ initiation varies considerably within the family (Pabón-Mora & González 2008). Thus Apostasioideae and Cypripedioideae have simultaneous initiation of members of the inner tepal whorl, the plesiomorphic condition for Asparagales (Kocyan & Endress 2001a); have Vanilloideae been studied?

Anthers of some species appear to be bisporangiate in early development (Freudenstein & Rasmussen 1996). At least some Orchidaceae have placentoids (Weberling 1989). Prutch and Schill (2000) discuss variation in the morphology and ultrastructure of the stigma; variation seems to be at about the subfamilial level. Kodahl et al. (2015) discuss embryo sac formation (6-nucleate embryo sacs are common in the family), double fertilization (extent unclear) and endosperm development (or lack thereof); see also Swamy (1949) and Wirth and Withner (1959). Although the seeds are generally minute and the testa cells have thin walls, Selenipedium (Cypripedioideae) has a hard, dark testa, although apparently it lacks phytomelan, while seeds of Vanilloideae are notably variable (Cameron & Chase 1998); see Barthlott et al. (2014) for a general seed survey.

For general information, see Schlechter (1992, 1996, 2003), Dressler (1993), and Szlachetko (1995); for accounts of Apostasioideae, see de Vogel (1969), Pridgeon et al. (1999) and Stern et al. (1993: anatomy). The series of volumes edited by A. M. Pridgeon, P. J. Cribb, M. W. Chase and F. N. Rasmussen deserve special notice - for Apostasioideae and Cypripedioideae, see Pridgeon et al. (1999), for Vanilloideae, Pridgeon et al. (2003), for Orchidoideae, Pridgeon et al. (2001b, 2003), and for Epidendroideae, see Pridgeon et al. (2005, 2009, 2014), representing as they do the synthesis of just about all available information. For terrestrial orchids, see Rasmussen (1999), and for an illustrated generic account, see Alrich and Higgins (2008). Anatomy: general, see Stern (2014), roots, see Moreira and Isaias (2008) and Siegel (2015), Epidendroideae, see Stern et al. (2004), Stern and Carlsward (2006, 2009), and Morris et al. (1996: Dendrobium), for Orchidoideae, see Stern (1997a, b), Stern et al. (1993b), and Andreota et al. (2015: Cranichideae), and for Apostasioideae, Stern et al. (1993a); the comprehensive ccounts edited by Pridgeon et al. mentioned above are also very useful. See also Pridgeon et al. (1983: tilosomes), Rasmussen (1987: stomata), Prychid et al. (2004: SiO2 bodies), Mayer et al. (2011: colleters, uncommon), Aybeke (2012: rhizome and roots of Orchidoideae and Epidendroideae, Limordorum rhizome with a ring of phloem surrounding a ring of xylem?), and Smidt et al. (2013: New World Bulbophyllum). For reticulate leaf venation in Vanilloideae, see Cameron and Dickison (1998).

See also Johansen and Frederiksen (2002: flowers), Endress (1994b: floral morphology), Kristiansen et al. (2001), Cameron (2002), Kurzweil (esp. 1987, 1993), Kocyan and Endress (2001a) and Kurzweil and Kocyan (2002), all floral development, Kurzweil (1998: useful summary of floral development), Bell et al. (2009: nectar spurs in Orchidoideae), Hirmer (1920: floral morphology), Swamy (1948a: floral vasculature), Rao (1973: floral anatomy), Valencia-Nieto et al. (2016: anther development, Epidendreae), Newton and Williams (1978: Cypripedioideae, Apostasioideae pollen), Schill and Pfeiffer (1977: pollen, general), Li et al. (2012: pollinia in Cypripedoideae), Freudenstein (1991: endothecium), Clements (1995: not read, embryology, etc.), Yeung and Law (1997: ovules and embryo sac), Kurzweil (2000), Molvray et al. (2000), Cameron and Chase (2000), Szlachetko and Rutkowski (2000) and Szlachetko and Margonska (2002), both gynostemium, Yeung (2005: embryogeny), Rasmussen and Johansen (2006: fruits).

Phylogeny. Cameron (2007) provided a summary of phylogenetic work on the family. With the advent of molecular studies, it was quite soon clear that the then current subfamilial limits were going to need adjustment (e.g. Kores et al. 1997). There may still be some uncertainty over the position of Cypripedioideae (e.g. Cameron 2004). In some analyses they grouped (albeit weakly) with Vanilloideae (Freudenstein & Chase 2001) or were sister to Orchidaceae minus Apostasioideae, which might make sense if thinking about androecial evolution (alone Cameron et al. 1999: one gene, successive weighting). However, they are often placed sister to Orchidaceae minus Apostasioideae and Vanilloideae (e.g. Kocyan et al. 2004; Cameron & Chase 2000; Cameron 2002, 2005b, 2006: two genes, in a basal trichotomy with atp alone; Górniak et al. 2010: nuclear gene Xdh; Givnish et al. 2015). This latter hypothesis, followed here, suggests that the monandrous condition may have evolved twice (see also Freudenstein et al. 2002, 2004). There are also suggestions that Codonorchis is sister to [Epidendroideae + Orchidoideae] (e.g. Clements et al. 2002) or basal in Orchidoideae (Cameron 2006: it has whorled leaves; c.f. Jones et al. 2002); the genus was sister to one of the two major clades that made up Orchidoideae in Givnish et al. (2015).

For phylogenies of Apostasioideae, see Kocyan et al. (2004) and Yin et al. (2016).

Relationships within Vanilloideae are becoming fairly well resolved (Cameron 2004, 2009; Cameron & Molina 2006; Pansarin et al. 2008). Included are Pogoniinae (Erythrorchis, a mycoheterotroph, is here), Vanillinae, and Galeolinae and Lecanorchidinae (both mycoheterotrophs). Pansarin et al. (2012) evaluated the phylogeny of Pogonieae; Pogoniopsis is to be placed in Epidendroideae. Bouetard et al. (2010) provide a phylogeny for Vanilla.

For relationships in Cypripedioideae, including also a morphological survey, see Albert (1994). Li et al. (2011) found morphology sometimes to have misled over relationships in Cypripedium; for a phylogeny of Paphiopedilum, see Chochai et al. (2012).

Orchidoideae include the erstwhile Spiranthoideae which have incumbent anthers (as in Epidendroideae) with apical rostellar tisssue. Relationships within Orchidoideae are becoming fairly well resolved (e.g. Cameron 2004); see also Inda et al. (2010: cox1 intron) anf Givnish et al. (2015). For relationships in Orchideae, see Bateman et al. (1997), Pridgeon et al. 1997), Inda et al. (2012) and Raskoti et al. (2016: Herminium and surrounds). For relationships within Orchidinae and Habenariinae, see Bateman et al. (2003), Habenaria was polyphyletic and Orchis triphyletic (the other bits are Anacampseros and Neottia), while in Asia, Habenaria is diphyletic and Platanthera triphyletic (Jin et al. 2014). New World species of Habenaria are monophyletic, although sectional limits need revision (Batista et al. 2013; Pedron et al. 2014). Clemens et al. (2002; see also Miller & Clements 2014; Weston et al. 2014) clarify relationships of Diuridae, a few of which are to be placed in Epidendroideae; for Codonorchis, see above. Disa is especially diverse in the Cape Region (see Bytebeier et al. 2007, 2008); for a phylogeny of Satyrium, see van der Niet and Linder (2008); it has diversified in the Fynbos region (Verboom et al. 2009). Prescottiinae s.l. have diversified at very high altitudes - up to 4,900 m - in the Andes (Álvarez-Molina & Cameron 2009). For information about relationships in the speciose Caladenia, see Australian J. Bot. 57(4). 2009, also Brown and Brockman (2015) for literature, for a study of Diuridae, Clements et al. (2002), of Pterostylis and relatives, see Clements et al. (2011), of the African Disa (Disinae), see Bytebier et al. (2007), and of the American Chloraeinae, see Cisternas et al. (2012). For the phylogeny of Cranichidae, see Salazar et al. (2003: monophyly and characters of subtribes, 2011a: comments on Spiranthinae), while Górniak et al. (2006) discuss relationships in Spiranthinae, Salazar et al. (2011a) examined relationships around Dichromanthus et al.; there adaptation to bird pollination has occurred in parallel, confusing generic limits, and Dueck et al. (2014) focussed on Spiranthes and its distribution.

For general phylogenetic relationships in Epidendroideae, see van den Berg (2005), Górniak et al. (2010) and especially Freudenstein and Chase (2015) and Givnish et al. (2015). Support for branching along the spine of Epidendroideae remains rather weak (e.g. Cameron et al. 1997; Pridgeon et al. 2001b; Cameron 2004), although less so in Givnish et al. (2016a). Palmorchis is sister to Neottieae, this clade of terrestrial orchids being sister to all other Epidendroideae (Rothacker & Freudenstein 2006; Freudenstein & Chase 2015). Xiang et al. (2012; see also Freudenstein 2012) found at least three more clades, including Sobralia and Elleanthus, Nervilia, and Tropidia respectively, to be successively sister to the rest at the base of the "higher", "upper" or crown epidendroids; they were in a single clade in some analyses of Freudenstein and Chase (2015), and Triphora makes another clade. Nervilieae and Tropidieae formed a single clade in Givnish et al. (2015), as did Triphoreae and Sobralieae. These "basal" taxa tend to lack articulated leaves, they have no velamen, their pollinia are sectile/mealy (Pridgeon et al. 2005), and many are ground-dwelling plants; if their position is confirmed, this will affect identification of apomorphies for the subfamily, and also for the highly speciose crown Epidendroideae, with eight or so tribes (Freudenstein & Chase 2015; Givnish et al. 2015).

For Sobralieae, see Neubig et al. (2011). Malaxis and Liparis (Malaxideae-Malaxidinae), both with terrestrial species in temperate as well as tropical regions, may not be monophyletic, but are closely intertwined (e.g. Cameron 2005a). For relationships in the Calanthe group (Collabieae), with plicate leaves and also largely terrestrial, see Zhai et al. (2014). Within Malaxideae-Dendrobiinae, the speciose Dendrobium and many of its sections are turning out to be polyphyletic (Yukawa & Uehara 1996: vegetatively variable, florally perhaps less so; Yukawa et al. 1993, 1996, 2000; Clements 2003: ITS study, see also earlier work). Bulbophyllum is relatively little studied, but see Gravendeel et al. (2004), Smidt et al. (2011) and B. Gravendeel, E. de C. Smidt, G. Fischer & J. J. Vermuelen in Pridgeon et al. 2014; Fischer et al. (2007) studied the Malagasy species and Hosseini et al. (2016: species from Peninsula Malaysia). For a major study of Epidendreae-Pleurothallidinae, see Pridgeon et al. (2001b); Pleurothallis is not monophyletic (Chiron et al. 2012: focus on Brazilian species). Abele et al. (2005) and Matuszkiewicz and Tukallo (2006) discussed the phylogeny of Masdevallia, Karremans et al. (2012) looked at relationships in Stelis, which has sometimes been extended to include "a few hundred" species of Pleurothallis and Karremans et al. (2016) looked at Specklinia and its immediate relatives. Sosa et al. (2016; see also Sosa 2007) discuss relationships within the terrestrial (and some mycoheterorophic) Bletiinae. Russell et al. (2010) discuss phylogeny in the widely-distributed Polystachya (Vandeae-Polystachyineae: monopodial), where there is some correlation of polyploidy with broad species distributions. Topik et al. (2005) investigated relationships in Aeridinae; characters conventionally used to establish relationships showed little congruence with the tree they obtained (see also Hidayat et al. 2005; Zou et al. 2015); for relationships in and around Vanda itself, see Gardiner et al. (2013). For angraecoid orchids (Angraecinae) in general, see Stewart et al. (2006), while Szlachetko et al. (2015: ITS) looked at relationships around Angraecum. For Epidendreae see Kulak et al. (2006). For phylogenetic relationships in Laeliinae, see van den Berg et al. (2000), in Pinheiro and Cozzolino( 2013) there is a summary of what is known about Epidendrum itself, while nuclear and plastid DNA give conflicting signals in Cattleya (van den Berg 2015). For diversification in Arethuseae-Coelogyninae, see Gravendeel et al. (2005), for studies in Maxillarieae, see Whitten et al. (2000), Williams and Whitten (2003), Sitko et al. (2006), Arévalo and Cameron (2013), and especially Whitten et al. (2007: Maxillaria to be restricted, generic realignments needed). For studies in Cymbidieae, see M.-H. Li et al. (2016: general, relationships [Cymbidiinae [Cyrtopodiinae + The Rest]], support in the middle part of the tree rather weak), Yukawa et al. (2002: Cymbidium), Whitten et al. (2005: Zygopetalinae), Neubig et al. (2008: Dichaea, Zygopetalinae), Cieslicka (2006), Martos et al. (2014) and Bone et al. (2015a, b), all Eulophia and relatives (Eulophiinae), and Chase (1987), Chase and Palmer (1997), Williams et al. (2001a, b, 2005), Chase et al. (2009) and especially Neubig et al. (2012a), all focusing on Oncidiinae and the polyphyletic Oncidium. Zhang et al. (2013) discuss relationships in Calypsoeae.

The recently described monotypic Pycnanthaceae from northwestern Argentina is indeed near Orchidaceae, as Ravenna (2011) suggested, but the description is poor (and the measurement units in the description are not always correct). The leaf sheaths are described as being closed, the flowers have a labellum, there are supposed to be three stamens with extrorse anthers, and the placentation is parietal. However, the type specimen looks like Malaxis (M. Chase, pers. comm. 2011) and that is where it is to be placed (Nicola 2012).

Classification. Chase et al. (2015; c.f. Chase et al. 2003) provide a higher-level phylogenetic classification for the family with practically all genera placed in the system, while Govaerts et al. (2003) is a provisional checklist (see also World Checklist of Monocots). For genera and synonymy in Apostasioideae, see Pridgeon et al. (1999), Cypripedioideae, Pridgeon et al. (1999), Vanilloideae, Pridgeon et al. (2003), Orchidoideae, Pridgeon et al. (2001b, 2003), and in Epidendroideae, Pridgeon et al. (2005, 2009, 2014).

Generic limits in the family are in the middle of a major overhaul to make them consistent with molecular findings, many of which have implications for clade/generic circumscriptions. In the past the importance of floral differences in separating genera was emphasized, but here, as elsewhere, there has been widespread homoplasy in floral features (e.g. Chase et al. 2009 and references), for example, the distinctive lip-like appendage that was a defining feature of the old Corycinae (Waterman et al. 2009) seems to have evolved in parallel. Szlachetko et al. (2005 and references) give a statement of the "floral" position, maintaining that variation in column form, etc., yields taxonomically important characters (see also Szlachetko 1995; Rutkowski et al. 2008). However, clade limits suggested by molecular studies and generic limits suggested by floral features alone by no means always agree (Kocyan et al. 2008 and references). The features characterising the erstwhile broadly-delimited and polyphyletic Oncidium - mimicry of oil flowers of Malpighiaceae, whether or not the orchid also offers oil as a reward - is a good example of this (Williams et al. 2001; Neubig et al. 2008; Stpiczynaska & Davies 2008; Chase et al. 2009; esp. Neubig et al. 2012a), similarly, in Aeridinae there is also probably widespread parallelism in floral characters used to delimit genera (Hidayat et al. 2005; Salazar et al. 2011a, b for other examples). It is not that floral morphology is inherently taxonomically useless, but undue reliance on it will lead us seriously astray if our interest is in understanding phylogeny. In some Epidendroideae vegetative variation may correlate better with clades evident in molecular phylogenies (e.g. Cameron 2005a), although anatomical variation by itself may suggest little major phylogenetic structure (Stern et al. 2004; Stern & Carlsward 2006).

There have been extensive discussions about generic limits in European Orchidinae (e..g. Bateman et al. 1997; Tyteca & Klein 2008, 2009; Bateman 2009; Scopece et al. 2010b; M. Kropf in Kadereit et al. 2016). In an attempt to make generic limits there more objective, Scopece et al. (2010b) found that clade membership correlated well with post-zygotic reproductive isolation (embryo death). A phylogeny-based classification in which this and other evidence was incorporated could, they thought, be defended on more explicit grounds, and this would allow morphologically distinctive taxa previously segregated as separate genera be incorporated into their proper clades (Scopece et al. 2010b). This approach is somewhat reminiscent of that of Danser (1929), and although perhaps useful in Orchidaceae - but it is going to be interesting to see how widely it can be applied even here, and what the taxonomic consequences are - it may be inapplicable to orchids with different breeding behaviours. For an account of Anacamptis, Orchis, etc., see Kretzschmar et al. (2007).

Disagreements over generic circumscriptions reflect fundamental differences in classificatory philosophies and differing beliefs in the ability of morphology when used alone alone to disclose relationships. However, even having a phylogeny and agreeing over basic taxonomic philosophy does not lead to automatic agreement about generic boundaries. Thus Clements (2003, 2006) suggested a wholesale pulverization and reorganization of generic limits in Dendrobium and its relatives. The species numbers given above do not reflect this, and Burke et al. (2008), Janes and Duretto (2010), Schuiteman and Adams (2011), and Schuiteman (2012) suggest that a broader circumscription of the genus would be preferable; species limits are also at issue here (Adams 2011: focus on Australia). Jones and Clements (2002a, esp. 2002b) divide Pterostylis; Clements et al. (2011) note that there are nine or so identifiable groups around here, although that may not quite be to the point. Since the monophyly of Pterostylis s.l. has been confirmed, the division is perhaps questionable (if one likes broadly-drawn generic limits), and indeed Janes and Duretto (2010) and Jones et al. (2010) suggest returning to the old circumscription of the genus (see also Clements in Chase et al. 2015). Jones et al. (2001) also dismember the monophyletic Caladenia and Clements et al. (2002) divide a monophyletic Corybas, as do Jones et al. (2002 - also much else). Such cases simply reflect conflicting preferences for narrow or broad genus limits, so they are something of a pain. In any event, in Australia, the result of nomenclatural changes made for these and other reasons is that about 45% of the species and subspecies in the entire orchid flora of some species acquired new generic names between 2000 and mid-2009 (Hopper 2009) - surely, this is Taxonomic Progress. Finally, Reveal (2012) came up with an earlier name for Epidendroideae (10 versus 58,500 hits - Google search iv.2012), although it seems to have slid back into blessed obscurity. One can but hope for sense.

For generic limits in Maxillariinae, c.f. Whitten et al. (2007) and Szlachetko et al. (2012) and in Habenariinae, see Batista et al. (2013 and references). Schuiteman and Chase (2015) adopted a broad circumscription for Maxillaria, interestingly, 19/42 generic names they placed in synonymy had been described in the last ten years. For a reclassification of Pleurothallidinae, see Pridgeon and Chase (2001), and although Pleurothallis was not monophyletic, c.f. Karremans et al. (2012), while Karremans et al. (2016) discuss the synonymy of Specklinia. This is a huge group, and sampling is still relatively very poor. There is some controversy over generic limits in the Masdevallia area, c.f. Luer (2006) and Pridgeon (2007), and reclassification of Maxillarieae is likely (Whitten et al. 2007); Blanco et al. (2007) made many new combinations. For generic limits around Angraecum, see Szlachetko et al. (2015), for those around Cattleya, see van den Berg (2014), for those around Bulbophyllum, see Pridgeon et al. (2014) and Vermuelen et al. (2014), and for an infrageneric classification of Vanilla, see Soto Arenas and Cribb (2010). Further changes are in the offing, as is clear from the discussion in Chase et al. (2015), especially in genera like Angaecum Habenaria, Coelogyne, etc..

I do not pretend to have dealt with hybridization in Orchidaceae satisfactorily, in particular hybridization by horticulturalists. Those interested should consult Sander's list of registered hybrids (Royal Horticultural Society 2008, also see the quarterly updates by the Society ("Quarterly Supplement to the International Register and Checklist of Orchid Hybrids (Sander's List)". Generic name changes can have considerable consequences here. Thus the acceptance of generic name changes in some Epidendroideae in Pridgeon et al. (2005) necessitated over 10,000 changes to the names of hybrids which had to be transferred to a hybrid genus other than the one in which they were originally registered (Royal Horticultural Society 2008).

[[Boryaceae et al.] [[Ixoliriaceae + Tecophilaeaceae] [Doryanthaceae [Iridaceae [Xeronemaceae [Asphodelaceae [Amaryllidaceae + Asparagaceae]]]]]]]: (stem fructans +); (cuticular waxes as platelets transversely arranged in parallel series); (T ± connate); (A inserted on T tube); tapetal cells bi- to tetranucleate; seeds exotestal, (phytomelan +).

Age. This node is dated to around (97-)89(-79) or 85.1 m.y.a. (S. Chen et al. 2013), about 102.9 m.y.a. (Magallón et al. 2015), and about 119 m.y. (Tank et al. 2015: Table S2).

Chemistry, Morphology, etc. For the distribution of fructose oligosaccharides, see Pollard (1982) and Meier and Reid (1982). Although recorded there only for some Hypoxidaceae in the [Boryaceae [Blandfordiaceae [Lanariaceae [Asteliaceae + Hypoxidaceae]]]] clade, and not for some of the smaller families elsewhere in Asparagales, fructans seem to be widespread in this part of the tree; they were not recorded from Orchidaceae.

[Boryaceae [Blandfordiaceae [Lanariaceae [Asteliaceae + Hypoxidaceae]]]]: septal nectaries external; ovules with hypostase; embryo sac with chalazal constriction, antipodal cells persistent.

Age. This node can be dated around (87-)67(-47) or 42/65.2 m.y. (S. Chen et al. 2013: last two numbers should be the same - c.f. Table 3), m.y. (Janssen & Bremer 2004: but c.f. topology) or ca 93.3 m.y.a. (Magallón et al. 2015).

There are many dates for clades in this area in both Janssen and Bremer (2004) and Wikström et al. (2001), but the topologies there differ from that above; if relationships change, some ages may be of use.

Chemistry, Morphology, etc. For some information, see Kocyan and Birch (2011); there is extensive homoplasy in this little clade, so exactly where features like "septal nectaries external" are to be placed is unclear.

Phylogeny. Relationships between Milligania and Lanaria and Blandfordia were suggested by Bayer et al. (1998a). Kocyan and Birch (2011: all genera studied) found that Lanariaceae, Asteliaceae and Hypoxidaceae formed a trichotomy, while Seberg et al. (2012) found that jackknife support for the clade was poor, and that Asteliaceae and Lanariaceae reversed their positions, i.e. to [Asteliaceae [Lanariaceae + Hypoxidaceae]], and relationships were also scrambled in Janssen and Bremer (2004) and Wikström et al. (2001).

BORYACEAE M. W. Chase, Rudall & Conran   Back to Asparagales


Plant xeromorphic, (growth monopodial - Alainia); aerial stems ± woody, rhizome short, (with stilt roots); roots mycorrhizal; endodermis much thickened; bundles with lateral phloem; leaves spiral, base sheathing; inflorescence scapose, involucrate, capitate; T tube short; A adnate to tube [not Alania]; anthers (centrifixed), little longer than wide; septal nectaries external; micropyle bistomal, parietal tissue 1 cell across; T persistent in fruit; (seed papillate - Borya); endosperm helobial, without starch, embryo short, ovoid; n = 11, 14; seedling?

2[list]/12. Australia, scattered (map: see Brittan et al. 1987). [Photo - Borya Habit © M. Fagg]

Age. Crown group Boryaceae are dated to 54 m.y. (Janssen & Bremer 2004).

Ecology & Physiology. Borya has tuberculate roots that may have the coil-forming Rhizoctonia fungus is them (c.f. Orchidaceae); the plant is arborescent and dessication-tolerant (e.g. Barthlott 2006) and has vessels with almost simple perforation plates in the stem (Carlquist 2012a).

Chemistry, Morphology, etc. The pedicels of Alania have several bracteoles.

Additional information is taken from Dahlgren et al. (1985) and Conran (1998), both general, and Conran and Temby (2000: floral morphology).

Previous Relationships. Genera of Boryaceae have often been included in Anthericaceae (= Asparagaceae-Agavoideae), as by Takhtajan (1997).

[Blandfordiaceae [Lanariaceae [Asteliaceae + Hypoxidaceae]]]: blade with distinct midrib; nucellar cap ca 2 cells across.

Age. The age of this clade is estimated at (98-)81, 74(-56) m.y. by Bell et al. (2010: note topology), at (79-)58(-35) or ca 38.3 m.y. by S. Chen et al. (2013), and about 84.5 m.y.a. by Magallón et al. (2015).

Phylogeny. An at most moderately well-supported - if consistently appearing - group (Rudall et al. 1998a; Chase et al. 2000a; Fay et al. 2000; Davis et al. 2004 - Lanariaceae not included; Graham et al. 2006; Chase et al. 2006; etc.).

Chemistry, Morphology, etc. See Conran and Temby (2000) for general information, especially about ovules.

BLANDFORDIACEAE R. Dahlgren & Clifford   Back to Asparagales


Rhizome short; chemistry?; velamen +; raphides 0; plant glabrous; leaves two-ranked, vernation flat-curved, sheath?; inflorescence a raceme; pedicels articulated; T large, tubular; (A adnate below middle of tube), anthers latrorse, centrifixed; pollen trichotomosulcate; G stipitate, septal nectaries on outside of ovary; style short, stigma ± punctate, dry; outer integument 3-4 cells across, hypostase +; capsule septicidal; exotesta papillate; embryo short; n = 17, 27; cotyledon photosynthetic.

1[list]/4. E. Australia (map: see Brittan et al. 1987). [Photo - Blandfordia Flower © B. Walters.]

Age. The age of this clade was estimated at (7-)4(-1.5) m.y. by S. Chen et al. (2013).

Evolution. Divergence & Distribution. Hardly a terribly diverse clade (Tank et al. 2015: Table S1).

Chemistry, Morphology, etc. Information is taken from Clifford and Conran (1998: general), Di Fulvio and Cave (1965) and Prakash and Ramsey (2000: both embryology) and Kocyan and Endress (2001b: some floral morphology.

Previous Relationships. Rudall (2003a) suggested that there was a close morphological relationship between Boryaceae and Blandfordiaceae.

[Lanariaceae [Asteliaceae + Hypoxidaceae]]: hairs multicellular, often branched; stomata paracytic; G ± inferior, septal nactaries internal; ovule with bistomal micropyle, micropyle zig-zag.

LANARIACEAE R. Dahlgren   Back to Asparagales


Plant with vertical rhizome; biflavones +; raphides 0 (styloids +); indumentum dendritic; leaves two-ranked to spiral, sheath ?closed; inflorescence branched; T connate half-way; A adnate in mouth; G ± inferior, style long, stigma punctate; ovules 2/carpel, apotropous, outer integument 5-7 cells across, parietal tissue ca 3 cells across, obturator +; capsule type?; seed 1; exotesta palisade, other cells rounded, tegmen persists, develops at micropyle; endosperm initially with starch; n = 18; seedling?

1[list]/1: Lanaria plumosa. Cape Province, South Africa. [Photo - Habit] [Photo - Habit.]

Evolution. Divergence & Distribution. There may have been a slowing of diversification in this clade (Hertweck et al. 2015, but c.f. topology).

Chemistry, Morphology, etc. Information is taken from De Vos (1963 - embryology), Dora and Edwards (1991 - chemistry) and Dahlgren (in Dahlgren & Van Wyk 1988) and Rudall (1998) both general.

[Asteliaceae + Hypoxidaceae]: plants rosette-forming or caespitose; flavonols +; mucilage canals +; ovules few to many/carpel; endosperm thin-walled; cotyledon not photosynthetic, ligule long.

ASTELIACEAE Dumortier   Back to Asparagales


Plant ± rhizomatous; saponins +; indumentum branched-lepidote-stellate; leaves 3-ranked, linear, ensiform, or subulate, base sheathing, closed, or not; plant dioecious (polygamodioecious, flowers perfect), inflorescence branched raceme or spike, inflorescence bracts large; flowers rather small, T connate basally (free) (10-14); staminate flowers: A (10-14), adnate to base of T/free; (nectaries on outside of ovary), pistillode +; pistillate flowers: staminodes +, (G subinferior), (5-7), (placentation parietal), intra-ovarian trichomes +, style branched or not (short), stigmas capitate to decurrent, dry; ?nucellar cap; fruit a berry; funicle distinct {= "long"], with ± well developed mucilaginous hairs; endosperm oily, no hemicellulose; n = 30, 35, ...105, chromosomes 4-6 µm long; seedling primary root well developed.

3[list]/31. New Zealand to New Guinea, Pacific Islands E. to Hawaii, Chile, the Mascarenes (map: see van Steenis & van Balgooy 1966; Fl. Austral. 45. 1987). [Photos - Milligania & Astelia Flowers © C. Howells - Australian Plants Society, Tasmania.]

Age. Crown-group Asteliaceae are dated to ca 92 m.y. (Janssen & Bremer 2004); Birch et al. (2012) date it to (76-)55.4(-36.0) m.y. and S. Chen et al. (2013) 32.6 or (51-)29.5(-12.5) m. years.

Fossils from New Zealand identified as stem-node Astelia are ca 23.2 m.y.o. (Iles et al. 2015).

Evolution. Divergence & Distribution. For the biogeography of the family see Birch et al. (2008, 2011, esp. 2012); there has been extensive long-distance dispersal, and Asteliaceae seem to have been around in New Zealand in the Oligocene, when the island was all or mostly under water... One species of Astelia is known from Réunion (see map). For the Mascarenes/Africa-Hawaii/Antipodes connection, see also Malvaceae (Kokia), Asteraceae (Hesperomannia); Keeley and Funk (2011) give a list of Hawaiian endemics, also see Acacia (Fabaceae).

Given current ideas of relationships in the family (see below), character evolution in it will repay investigation.

Chemistry, Morphology, etc. Carlquist (2012a) suggested that vessels were practically absent, except perhaps in the roots - although this might depend on the technique used to prepare the material.

For additional information, see Prakash and Ramsey (2000: embryology), and Brittan et al. (1987) and Bayer et al. (1998a), both general, for information.

Phylogeny. The phylogeny of the family has been clarified by Birch et al. (2009); Milligania, with loculical capsular fruits, a semi-inferior ovary and no intra-ovarian trichomes, perfect flowers, etc., and often considered rather different from other Asteliaceae, seems to be embedded in Astelia, as do the other small genera previously recognized in the family (Birch et al. 2008, esp. 2009). However, Birch et al. (2012) found the relationships [[Neoastelia + Milligania] The Rest].

Classification. Astelia is to include Collospermum (Birch et al. 2012); for an infrageneric classification of the latter, see Birch (2015).

HYPOXIDACEAE R. Brown, nom. cons.   Back to Asparagales


Stem ± cormose to rhizomatous, leaf bases persisting, contractile roots common; fructan sugars accumulated, saponins 0; velamen +, dimorphic root hypodermis 0; stomata (tetracytic), with oblique or parallel cell divisions; leaves 3-ranked, (vernation conduplicate-)plicate (conduplicate-flat), (unifacial), sheaths also closed; inflorescence various, scapose, axis flattened; (flowers 2-merous); T free to long-tubular; (A inserted towards base), (many), (3, plus 3 staminodes adnate to style [= gynostemium] - Pauridia), (extrorse), (basi- or centrifixed, sagittate); tapetum amoeboid, microsporogenesis successive [tetrads tetragonal]; (pollen to trisulcate [Pauridia], inaperturate); ovary inferior, (apical beak +), septal nectaries 0, (placentation parietal - Empodium), stigmas commissural, ± 3-radiate, dry or wet; ovules apotropous, (outer integument to 4 cells across), (nucellar cap 0), (parietal tissue 0); (embryo sac bisporic, 8-celled [Allium type]), antipodal cells soon die; fruit dehiscing laterally, loculicidal, (circumscissile), indehiscent, or baccate, (with a long beak [= persistent corolla tube]); seeds globose, smooth to spiny, (strophiole +); exotesta palisade or not, (endotegmen persistent), raphe prominent; endosperm nuclear to helobial, (perisperm +, slight); n = 6-9, 11, chromosomes 2-5 µm long; embryo short, ± undifferentiated.

7-9[list]/100-220: Hypoxis (50-100), Pauridia (31). Seasonal tropics, esp. southern Africa (temperate) (map: see Fl. N. Am. 26: 2002; Australia's Virtual Herbarium xi.2012). [Photo - Inflorescence, Flower.]

Age. Crown group Hypoxidaceae have been dated to as much as ca 78 m.y.a. (Janssen & Bremer 2004) and as little as (33-)23(-16) or ca 15.6 m.y. by S. Chen et al. (2013).

Evolution. Pollination Biology & Seed Dispersal. Pollen is the main reward, and flies of various kinds, beetles and bees seem to be the pollinators (Kocyan et al. 2011 for a summary). At least some species of Hypoxis are apomictic (Nordal 1998).

Chemistry, Morphology, etc. Kocyan (2007) found that some flowers of Curculigo racemosa were polyandrous, however, the stamens were not fasciculate. The staminodes of Pauridia that are adnate to the style rather surprisingly appear to represent the outer androecial whorl - and they are responsible for reports of a 6-lobed stigma in the family. The rostrum, a narrowed, beak-like apical part of the ovary, appears to have evolved more than once, but its function is uncertain; the beak may also be formed by the connate tepals.

There is controversy over the tapetum type in the family and in the numbers of nuclei in the cells, and whether or not there is a velamen in the root. The ovules have a parietal cell, so are not tenuinucellate [?incorrect - not in the literature I have read]. The endosperm is reported as being nuclear or helobial; if the former, then the antipodal cells tend to persist (de Vos 1948, 1949).

Additional information is taken from Nordal (1998), Judd (2000) and Wiland-Szymanska (2009: east Africa), all general, Rudall et al. (1998a: anatomy), Thompson (1976: vegetative; 1978 floral morphology), Kocyan and Endress (2001b: floral morphology), Stenar (1925: embryology), and and Arekal (1967: ovule and seed).

Phylogeny. Kocyan et al. (2011) recovered three main clades - Curculigo et al., Pauridia et al., and Hypoxis - in the family, a slight modification of the results obtained by Rudall et al. (1998). Relationships between these clades was unclear.

Classification. For generic limits, see Kocyan et al. (2011) and Snijman and Kocyan (2013).

Previous Relationships. Rudall (2003a) suggested that there might be a close morphological relationship between Hypoxidaceae and Orchidaceae. In older classifications, Hypoxidaceae were included in Amaryllidaceae.

[[Ixoliriaceae + Tecophilaeaceae] [Doryanthaceae [Iridaceae [Xeronemataceae [Asphodelaceae [Amaryllidaceae + Asparagaceae]]]]]]: ?

Age. The age of this node is estimated at ca 84 m.y. by Eguiarte (1995), (98-)87, 78(-68) m.y. by Bell et al. (2010), ca 80 (Fig. 3), m.y. by S. Chen et al. (2013), and around 89 m.y.a. by Magallón et al. (2015).

[Ixioliriaceae + Tecophilaeaceae]: cormose; leaves spiral, shortly cylindrical at apex [Vorlauferspitze], base sheathing; flowers quite large; outer T mucronate to aristate, T tube short; A inserted at mouth of tube; embryo long; x = 12.

Age. For the age of this node, some (93-)79, 70(-59) m.y., see Bell et al. (2010), while (79.3-)64.1(-46.5) or ca 34.1 m.y. is the estimate in S. Chen et al. (2013) and ca 79.7 m.y. in Magallón et al. (2015). The divergence of Ixoliriaceae is dated to ca 112 m.y. and that of Tecophilaeaceae to 108 m.y. (Janssen & Bremer 2004: note topology).

Evolution. Divergence & Distribution. The rate of diversification may have slowed in this clade (Hertweck et al. 2015: all three).

Chemistry, Morphology, etc. The outer tepals in at least some Iridaceae (and Orchidaceae!) are also mucronate to aristate.

Phylogeny. There is weak to moderate support for this taxon pair in Chase et al. (2000a), Pires et al. (2006), Givnish et al. (2006) and Seberg et al. (2012), and stronger support in Graham et al. (2006: sampling poor); they have a very long branch in the three-gene analysis of Fay et al. (2000). Davis et al. (2004) found some support for the clade [Ixoliriaceae + Iridaceae], although sampling was poor; Chase et al. (2006) found strong support for this relationship. Janssen and Bremer (2004) found pectinate relationships here: [Ixoliriaceae [Tecophilaeaceae [Doryanthaceae + the rest]]], while the relationships [Tecophilaeaceae [Doryanthaceae [Ixoliriaceae + Iridaceae]] the rest] in Chase et al. (2006) had very little support.

Previous Relationships. Both Dahlgren et al. (1985) and Takhtajan (1997) recognised relationships between Ixoliriaceae and Tecophilaeaceae, as well as with a selection of other asparagalean families.

IXIOLIRIACEAE Nakai   Back to Asparagales


Plant a tunicated corm; saponins 0?; dimorphic exodermis 0; peduncle with a sclerenchymatous ring; mucilage cells +; leaf base ?type; inflorescence subumbellate, leafy; T tube short; A centrifixed; tapetal cells uninucleate; ovary inferior, stigma 3-lobed, dry; outer integument 3-4 cells across, parietal tissue ca 2 cells across, nucellar cap ca 2 cells across; fruit ?type; seeds angled, phytomelan +; endosperm walls pitted, starch in cells surrounding embryo; cotyledon remains white even when exposed to light!

1[list]/3. Egypt to Central Asia (map: from Traub 1942, rather approximate). [Photo - Flower © A. Shoob]

Chemistry, Morphology, etc. The vascular bundles in the leaf are unequal in size, some in the inflorescence axis are arranged in a circle, enclosing additional scattered bundles.

Information is taken from Kubitzki (1998b: general), Arroyo (1982) and Arroyo and Cutler (1984: both anatomy), Dönmez and Isik (2008: pollen), Stenar (1925: embryology), and Tillich (2003: seedling morphology).

Previous Relationships. The inflorescence axis is leafy, the flowers are blue and there are no alkaloids, all unusual features for Amaryllidaceae, where Ixiolirion was often included (Takhtajan 1997).

TECOPHILAEACEAE Leybold, nom. cons.   Back to Asparagales


Corm, tunicated, (in vertical series), (tuber); ?saponins +, fructan sugars accumulated [Cyanastrum]; stomata variable; leaf with petiole and blade, more than one order of parallel veins, (transverse veins branching, reticulated), sheaths closed (none); inflorescence a raceme, branched or not, or flowers axillary; (bracteoles 0); flowers monosymmetric (polyusymmetric), (axillary); (T tube moderately long); (stamens of very different sizes), (stamens 4-3, staminodes 2-3), anthers dehiscing ± by pores; pollen operculate (not Kabayea and Cyanastrum); (G semi-inferior; carpels free - Cyanastrum), stigma punctate; ovules 2-many/carpel, ana-campylotropous, outer integument "thick", vascularized [Cyanastrum], obturator +; seed (one/fruit), phytomelan +, (0, surface warty, with tufts of small hairs), testa multilayered, (exotesta palisade), thick-walled; endosperm (nuclear - Cyanella), thick-walled, pitted or not, (± absent), ?starch (0, chalazosperm + - Cyanastrum), embryo also short; n = 8, 10-12, 14, chromosomes 2-4 µm long; cotyledon not photosynthetic, (coleoptile +), primary root long (hypocotyl and primary root 0 - Cyanastrum).

7[list]/25: Cyanella (9). Africa, Chile, and the U.S.A. (California - Odontostomum) (map: from Carter 1962; Scott 1991; Brummitt et al. 1998; Fl. N. Am. 26: 2002). [Photo - Flower, Flower.]

Age. Crown-group Tecophilaeaceae have been dated at ca 87 m.y. (Janssen & Bremer 2004), ca 77 m.y.a. (Buerki et al. 2013a), and (41-)30(-20) or ca 20.4 m.y. (S. Chen et al. 2013).

Evolution. Divergence & Distribution. Buerki et al. (2013a) discussed the complex eco-biogeographical history of this small clade, i.a. they noted that its colonization of what are now Mediterranean ecosystems occurred before the origin of the Mediterranean climate, as seems to be common (see also Vargas et al. 2014).

Chemistry, Morphology, etc. This is a heterogeneous group. Cells adjacent to stomata in Cyanastrum were described as having parallel cell divisions by Tomlinson (1974).

The monosymmetry of the flower is largely caused by the androecium; enantiostyly also occurs in a few species of Cyanella. Odontostomum has been reported to have six staminodia alternating with the six stamens; the "staminodia" are some kind of corona or other enation from the tepals.

Some information is taken from Dahlgren (in Dahlgren & van Wyk 1988), Rudall (1997), Simpson and Rudall (1998), Brummitt et al. (1998) and Manning and Goldblatt (2012); for ovules, see Nietsch (1941), and for seedlings, variable in morphology, see Tillich (1996a, 2003).

Phylogeny. Tecophilaea was found to be sister to the rest of the family, although with only moderate support; other relationships along the backbone were poorly resolved (Brummitt et al. 1998). More recently, Buerki et al. (2013a) found that the clade [Conanthera + Zephyra] (both genera are from South America) were sister to the rest of the family.

Classification. Given the poor support for many relationships here, a classification is premature (c.f. Brummitt et al. 1998); despite a more resolved phylogeny, Buerki et al. (2013) quite reasonably elect not to develop any formal suprageneric hierarchy.

Synonymy: Androsynaceae Salisbury, Conantheraceae Pfeiffer, Cyanastraceae Engler, Cyanellaceae Salisbury, Walleriaceae Takhtajan

[Doryanthaceae [Iridaceae [Xeronemataceae [Asphodelaceae [Amaryllidaceae + Asparagaceae]]]]]: ?

Age. this node has been dated to ca 107 m.y.a. (Janssen & Bremer 2004); the separation of Doryanthaceae from Iridaceae (sic) has been estimated at ca 82 m.y.a. (Goldblatt et al. 2008).

Pollen fossils assigned to Iridaceae-Isophysis or to Doryanthes have been found in Late Cretaceous rocks ca 75-70 m.y. old from Eastern Siberia (Hoffmann & Zetter 2010).

Phylogeny. There is only moderate support for this position in Fay et al. (2000) and practically no support in Seberg et al. (2012), but 92% bootstrap support in Graham et al. (2006: note sampling); see also Janssen and Bremer (2004).

DORYANTHACEAE R. Dahlgren & Clifford   Back to Asparagales


Huge sub-bulbous tufted perennial; steroidal saponins +; vascular bundles encased in fibres; styloids +, raphides 0; cuticular wax rodlets parallel, stomata paracytic, subsidiary cells with oblique divisions; leaves spiral, apex cylindrical [Vorlauferspitze], when older as dry threads; inflorescence with inflorescence bracts, (subumbellate); T large, with two rows of vascular bundles, apex, esp. of outer T, cucullate, tube long; (A also adnate to the base of the tepal lobes), anthers latrorse, centrifixed, endothecium thick; pollen trichotomosulcate, surface reticulate; ovary inferior, stigma punctate, dry; ovules in two ranks, outer integument ca 5 cells across, inner integument ca 2 cells across, parietal tissue ca 5 cells across, nucellar cap ca 2 cells across, postament +; antipodal cells to 5, ± persistent; seeds flattened, winged; testa multiplicative, many-layered, with phlobaphene; endosperm helobial, thin-walled, embryo flattened; n = 17, 18, 22, 24, bimodal; seedling with laterally compressed haustorium, coleoptile +.

1[list]/2. E. Australia (map: from O. Seberg, pers. comm). [Photo - Habit.]

Age. The divergence of the two species in the family is estimated to have occured (8-)4(-1) m.y.a. (S. Chen et al. 2013).

Chemistry, Morphology, etc. Kocyan and Endress (2001b) note that the connective is massive, each stamen being supplied by 2-4 "vascular complexes", although these were not observed by Newman (1928, 1929). There may be a hypostase immediately beneath the embryo sac, although there is also a great amount of tissue between it and the chalazal bundle (Newman 1928).

Much general information is taken from Wunderlich (1950) and Clifford (1998); Blunden et al. (1973) described leaf anatomy, and Tillich (2003) described seedling morphology.

Iridaceae [Xeronemataceae [Asphodelaceae [Amaryllidaceae + Asparagaceae]]]: (vegetative fructans); (monocot secondary thickening +); (seeds with glucomannans as reserves); Arabidopsis-type telomeres lost, (TTAGGG)n [human-type telomeres] common.

Age. This node is estimated at (92-)81, 72(-62) m.y.o. by Bell et al. (2010), (83-)75(-65) or ca 51.2 m.y.o. by S. Chen et al. (2013), about 80.7 m.y.a. by Magallón et al. (2015) and about 98.1 m.y. by Tank et al. (2015: Table S2).

Evolution. Vegetative Variation. A distinctive pattern of secondary growth is scattered in this clade, and it has also been reported from Eriocaulaceae (Poales: Scatena et al. 2005). A meristem cuts off tissue to the inside, where separate vascular bundles embedded in ground tissue differentiate (Tomlinson 1970; Tomlinson & Zimmermann 1969; Zimmermann & Tomlinson 1972; Rudall 1991, 1995b for records and literature). It can be thought of as the continued activity of the primary thickening meristem (see also Cheadle 1937 Carlquist 2012a). Although there is sometimes a transition from collateral to amphivasal vascular bundles as the secondary thickening phase takes over, this is by no means always so (e.g. Diggle & DeMason 1983; Rudall 1984). Inflorescences are terminal, as in most other monocots, and so there is branching, and there are complex patterns of branching and fusion of bundles of the stem and branch (Haushahn et al. 2014). Mangin (1882) had suggested there might be a connection between the origin of this secondary thickening and the reticulum of vascular bundles in association with which "adventitious" roots arise in monocots.

Genes & Genomes. The loss of Arabidopsis-type (A-type) telomeres is not simple; human-type telomeres ((TTAGGG)n) may predominate, but there are other types, too. Asparagaceae-Scilloideae agree with other members of this clade, although the A-type telomere is somewhat more common than in the other members sampled (Adams et al. 2001; especially Sýkorová et al. 2003b, 2006a, b). Acanthocarpus, alone among the taxa discussed there as being an out-group, also lacks A-type telomeres, but it is in fact a member of Asparagaceae-Lomandroideae (ex Laxmanniaceae), an ingroup, not Dasypogonaceae, a commelinid.

Chemistry, Morphology, etc. The plants may have distinctive carbohydrates (Meier & Reid 1982; Buckeridge et al. 2000a). Apparently there are only tracheids in the xylem (Fahn 1990).

Glucomannan seed reserves are scattered in this clade, being associated with thick-walled endospermal cells, but I do not know details of their distribution. They are reported from Iridaceae, Amaryllidaceae-Allioideae, Asparagaceae-Asparagoideae and -Scilloideae-Ornithogaleae - and they are also known from some Liliales (see e.g. Elfert 1894; Jakimow-Barras 1973; Reid 1985).

Phylogeny. A group with quite strong support in Fay et al. (2000) and Soltis et al. (2007a), etc., but lacking much jackknife support in Seberg et al. (2012: bootstrap support better).

IRIDACEAE Jussieu, nom. cons.   Back to Asparagales


Plant rhizomatous; roots mycorrhizal; flavone C-glycosides, flavonols +, chelidonic acid 0?; dimorphic root hypodermis +; (stem endodermis +); raphides 0, styloids +; cuticular wax rodlets parallel; leaves two-ranked, isobifacial [oriented edge on to the stem], (vernation plicate); flowers usu. large; T ± free, apex often aristate; A 3, opposite outer T, extrorse, endothecial cells with U-shaped thickenings; G opposite outer T, septal nectary 0, style branched (branches bifid), stigma on the edges of the complex/expanded branches, dry; micropyle endo- or exostomal, outer integument 4-6 cells across, parietal tissue 1(-2) cells across (absent); seed testal and tegmic, phytomelan 0, phlobaphene +, endotesta pigmented, with lipids; endosperm thick-walled, hemicellulosic, embryo quite large; cotyledon not photosynthetic, (hypocotyl short).

66[list]/2105 (?2155) - eight subfamilies below. World-wide (map: see Heywood 1978 [S. America], Hultén & Fries 1986; Mathew 1989; Fl. N. Am. 26: 2002; Bahali et al. 2004; FloraBase 2005; Davies et al. 2005: Fig. 2b suggests that Iridaceae grow throughout Africa, much of the Arabian Peninsula, etc...; Rodrigues & Sytsma 2006; Alexeyeva 2008). [Photos - Collection.]

Age. Crown group divergence is estimated to have begun ca 96 m.y.a. (Janssen & Bremer 2004), 70 or 66 m.y.a. (Goldblatt et al. (2008), or (68-)58.5(-49) or 51.2 m.y.a. (S. Chen et al. 2013).

1. Isophysidoideae Thorne & Reveal

Vessel elements in roots with scalariform perforation plates; biflavonoids [amentoflavone] +; crystals 0 [leaves]; flower solitary, with spathes; endothecium with radially elongated walls; microsporogenesis?; G [3], style shortly lobed, branches commissural; endosperm ?helobial; n = ?; seedling?

1/1: Isophysis tasmanica. Tasmania.

Synonymy: Isophysidaceae F. A. Barkley

[Iridoideae [Patersonioideae [Geosiridoideae [Aristeoideae [Nivenioideae + Crocoideae]]]]]: xanthone + [mangiferin], inflorescence with cymose units [flowers from the axils of successive prophylls, so they alternate = a rhipidium]; flowers short lived [open ca 1 day]; (pollen operculate [often with two exine bands in a sulcus]); G inferior; ovules 1-many /carpel; endosperm nuclear.

Age. The age of this node is around 62 m.y. (Goldblatt et al. 2008).

2. Iridoideae Eaton

(Plant bulbous); γ-glutamyl peptides, meta carboxy aromatic amino acids +; vessel elements in root with simple perforation plates, (vessels in stems and leaves - Sisyrinchium); (leaf vernation plicate); rhiphidia simple; (flowers long-lived; monosymmetric; T whorls strongly differentiated (not), (inner whorl bearded - some Iris); (A 2 - Diplarrena); T nectaries +, (oil glands or oil hairs +); endothecial cells with spiral thickenings [not Sisyrinchium]; (pollen grains with encircling aperture); (septal nectaries + - Diplarrhena), style branches long, tubular, (branches commissural - Sisyrinchium et al.); seedling (with ligule or coleoptile - e.g. Tigridia), (photosynthetic - e.g. Sisyrinchium)n = 6<.

Ca 30/890: Iris (350), Moraea (200), Sisyrinchium (60-260), Tigridia (50). Worldwide, but esp. the spine of Central and South America.

Age. Diplarrena separated from the rest of the subfamily ca 57 m.y.a. (Goldblatt et al. 2008).

[Patersonioideae [Geosiridoideae [Aristeoideae [Nivenioideae + Crocoideae]]]]: rhipidia 2, fused [binate], each unit with 2-many flowers; T connate; extra codon in rps4 gene.

Age. The age of this node is about 70 or 55 m.y. (Goldblatt et al. 2008).


3. Patersonioideae Goldblatt

Plant ± woody and rhizomatous; biflavonoids [amentoflavone] +; monocot secondary thickening +; vessel elements in roots often with scalariform perforation plates; inner tepals reduced to scales or 0; endothecial cells with base-plate thickenings, filaments ± connate; pollen spherical, inaperturate, intectate; stigma lobes broad; ovules apparently uniseriate; embryo small; n = 11, 21; two extra codons in rps4 gene.

1/24. More or less open conditions, scattered in Malesia, New Caledonia, and the periphery of Australia (map: partly from Fl. Austral. 46. 1986).

[Geosiridoideae [Aristeoideae [Nivenioideae + Crocoideae]]]: ?

Age. This node is about 48 m.y.o. (Goldblatt et al. 2008).

4. Geosiridoideae ("Geosiridaceae") Goldblatt & Manning

Plant echlorophyllous, mycoheterotrophic; crystals 0 [leaves]; leaves heterobifacial; flowers sessile; T connate basally only; microsporogenesis successive; ovules with outer integument 2-3 cells across, parietal tissue 1-2 cells across; seeds minute, dust-like, mesotesta 0; endosperm helobial, starchy, walls thick, hemicellulosic, embryo small; n = ?

1/2. Madagascar, the Comores.

Synonymy: Geosiridaceae Jonker

[Aristeoideae [Nivenioideae + Crocoideae]]: ?

Evolution. Divergence & Distribution. The age of this node is estimated at around 40 m.y. by Goldblatt et al. (2008) and (49-)34, 31(-17) m.y. by Bell et al. (2010).

5. Aristeoideae Vines

Plumbagin +; vessel elements in roots often with scalariform perforation plates; leaf bundles embedded, marginal sclerenchyma 0; T connate basally only; outer integument 2-3 cells across [?all]; embryo small; n = 16.

1/55. More or less open conditions, sub-Saharan Africa and Madagascar.

[Nivenioideae + Crocoideae]: flowers long-lived; septal nectary +.

Age. The age of this node is ca 36 m.y. (Goldblatt et al. 2008).

6. Nivenioideae Goldblatt

Plant with woody stem; monocot secondary thickening +; vessel elements in roots with scalariform perforation plates only; leaves with non-vascular fibrous strands; unit of rhipidium with 1-2 flowers; flowers long-lived, sessile; P long-tubular, T clawed (short-tubular, T long-linear - Klattia); endothecial cells with basal anastomosis of U-shaped thickenings; (pollen grains with encircling sulcus); stigmas simple, not or somewhat expanded; ovules 2/carpel (-6), endostomal, outer integument 2-3 cells across; 1 shield-shaped seed per loculus [seed tangentially flattened]; exotesta transparent, mesotesta 0-1 cell across; n = 16.

3/14. Only in the S.W. Cape region, South Africa

6. Crocoideae G. T. Burnett

Plant with corms; vessel elements in root with simple perforation plates; (mesophyll cells laterally elongate); (leaf vernation plicate), when flat with pseudomidrib (not Pillansia), sheath closed; inflorescence spicate; rhipidium binate, with a single flower, pedicel 0; (flowers short-lived), variously monosymmetric (polysymmetric); endothecial cells with spiral thickenings; pollen exine tectate, perforate-scabrate, aperture with one or a pair of longitudinal bands forming operculum, (zona-aperturate), (spiraperturate); (septal nectaries 0); (ovules campylotropous), nucellar columella +, hypostase prominent, postament +; chalazal endosperm haustorium +; n = 3-17, etc.

28/1005: Gladiolus (260), Romulea (90), Geissorhiza (85), Crocus (100 [?150]), Hesperantha (80), Babiana (55), Watsonia (50), Ixia (50). Overwhelmingly southern African, to Europe, Madagascar and Central Asia.

Age. Crown-group Crocoideae are only ca 24 m.y.o. (Goldblatt et al. 2008).

Synonymy: Crocaceae Vest, Galaxiaceae Rafinesque, Gladiolaceae Rafinesque, Ixiaceae Horaninow

Evolution. Divergence & Distribution. It is suggested that Iridaceae were originally from Antarctica-Australia, the family achieving its current distribution by a mixture of long-distance dispersal across a proto-Indian Ocean and migration via west Antarctica to Africa and the New World where the family is currently very diverse (e.g. Sanmartín & Ronquist 2004; Golblatt et al. 2008).

Davies et al. (2005) noted that in Iridaceae diversification was greater in areas like southern Africa than in the northern hemisphere, and there were clades with a disproportionately large number of species in e.g. southern Africa. The Cape area is notably diverse from a global point of view (Kreft & Jetz 2007), and Iridaceae are one of the major geophytic groups of the Cape (Procheŝ et al. 2006) with more than 650 species there, or 1,050 species in southern Africa as a while (Johnson 2010), the great majority of these species having specialized pollination (Goldblatt & Manning 2006). Davies et al. (2004c) see this diversification as the result of the interaction of local features such as the ecological and climatic heterogeneity of the area affecting reproductive isolation. Valente at al. (2012) suggested that pollinator shifts had helped drive speciation in southern African Gladiolus, although other factors were also involved. For the radiation of the Cape genus Moraea, both cytologically and florally diverse, see Goldblatt et al. (2002); radiation in this and other iridaceous Cape genera may have begun in the fynbos in the Miocene some 25 m.y.a., divergence in the succulent Karoo being more recent (Verboom et al. 2009). Diversification of two geophytic Cape genera, Babiana, with ca 92 species nearly all from the Greater Cape floristic region, and Moraea, with over 150 species in Cape region, may in part be connected with soil type preferences changing during speciation; here diversification began a mere 17-15 m.y.a. in the mid-Pliocene (Schnitzler et al. 2011); diversification rates in the Cape region and outside are largely similar (Silvestro et al. 2011).

Manning and Goldblatt (1991) suggest apomorphies for Nivenioideae.

Pollination Biology & Seed Dispersal. Iridaceae show considerable floral diversification, ranging from the open flowers of Sisyrinchium to the meranthia of Iris et al. (for which, see Guo 2015b) and the tubular flowers of Gladiolus et al. (e.g. Bernhardt & Goldblatt 2006; Goldblatt & Manning 2006 and references; Rodrigues & Sytsma 2006; Wilson 2006). In Iris and its relatives the flower will appear to the pollinator as if were really three monosymmetric flowers (e.g. Westerkamp & Claßen-Bockhoff 2007). The tepaloid style overarches the stamen opposite it and the landing platform for the pollinator is a member of the outer perianth whorl that lies directly underneath the style/stamen complex. However, in Cypella the three landing platforms for the pollinating bee are members of the inner perianth whorl. Here the pollen deposited on the backs of the bees comes from half anthers of adjacent stamens and is deposited on the receptive surfaces of two adjacent half-stigmas (Vogel 1974).

The flowers of Gladiolus (Crocoideae) are obliquely monosymmetric, although this is hardly apparent in the open flower due to changes in orientation as the flower and inflorescence grow. Tepal patterning, where it occurs, is usually on an adaxial lateral member of the outer whorl and adjacent members of the inner tepal whorl and is clearly on the adaxial side of the flower, but it may be on an adaxial lateral and the abaxial member of the outer whorl and a tepal of the inner whorl between them (Eichler 1875; Choob 2001). Although other Crocoideae may have the same oblique monosymmetry, Lapeirousia and Ixia, for example, have monosymmetric flowers with normal monocot orientation. Flowers in Diplarrena (Iridoideae) are similar, but they have only two stamens and one staminode. Interesting infraspecific variation occurs. In some flowers of Crocosmia X crocosmiiflora the odd member of the outer whorl was adaxial while in others it was abaxial; the patterning of the tepals, etc., varied accordingly (pers. obs.). All told, well over half the family has monosymmetric flowers of one sort or another, and the evolution of monosymmetry in the family will repay further study (see also Davies et al. 2004b).

Much work on pollination in Iridaceae has been carried out by Peter Goldblatt and John Manning, species from the sub-Saharan region, especially in South Africa, being the focus of their research. Nearly all species are morphologically specialized and are pollinated by non-specialist (if sometimes highly specialized) pollinators (Goldblatt & Manning 2006, 2008 for general accounts; Johnson 2010). Floral homoplasy is very extensive in Iridoideae-Tigridieae (Rodrigues & Sytsma 2006), -Trimezieae (Lovo et al. 2012), and -Irideae (in Iris itself - Wilson 2006). Many different kinds of pollinator are involved. Thus Babiana (Crocoideae) is pollinated by birds, scarab beetles, bees, moths, etc. (Bernhardt & Goldblatt 2006; esp. Goldblatt & Manning 2007), while scarabeid monkey beetles pollinate the flowers of three Cape genera of Iridaceae that have distinctive dark markings at the bases of the tepals (van Kleunen et al. 2007). Valente at al. (2012) examined pollination in southern African Gladiolus, recording numerous gains and losses of 5/7 of the pollination syndromes (the other two were decidedly uncommon), with long-tounged bee pollination being acquired at least four or twelve times (depending on the method used), but lost twice as frequently or more, while there were 17 pollinator shifts in the 23 species of Lapeirousia studied (Forest et al. 2014: mor important in speciation that changes in substrate specificity). For a discussion on the evolution of the complex appendages, etc., on the sepals of bearded irises and their ilk, see Guo (2015a, b).

At least 34 species of southwest African Iridaceae are known to be pollinated by three species of (extremely) long-tongued dipteran nemestrinid flies, and all told slightly over 10% (117 species) of the 1,025 species of Iridaceae in southern Africa have such pollinators. The long-tubed monosymmetric flowers pollinated by these flies have evolved several times here as well as in unrelated groups (Manning & Goldblatt 1996, 1997; Goldblatt & Manning 2000, 2006), and Karolyi et al. (2013) discuss how the flies take in the nectar. This compares with a mere 64 species of Iridaceae in the same region that are bird pollinated and over 550 species that are pollinated by long-tongued Apidae (Goldblatt & Manning 2006). There are a number of oil flowers in Iridaceae, including Cypella (see above), ca 35 species of Sisyrinchium from South America, and some other New World Iridoideae like Tigridia (Renner & Schaefer 2010); oil-secreting trichomes appear to have evolved twice in Sisyrinchium alone (Chauveau et al. 2011). Indeed, these trichomes vary both in morphology and position in flowers of New World Iridaceae (Silvério et al. 2012); evolution of floral rewards in these taxa has a complex pattern of gains, changes and losses (Chauveau et al. 2012).

Some species of Nivenia are heterostylous, a very uncommon condition in the monocots.

Vegetative Variation. Some Iridaceae are more or less woody and have monocot-type secondary thickening; the vessel elements in the roots of such plants often have predominantly scalariform perforation plates (Cheadle 1964: inc. Klattia). Foliar variation is considerable. Leaves may be terete and unifacial or apparently ordinary and heterobifacial (e.g. some Iris). Very commonly they are ensiform and isobifacial, as in Gladiolus and most Iris, are while others are like Crocus can be strangely ribbed, in transverse section they all seem to be modifications of a basic isobifacial leaf theme (e.g. Ross 1892, 1893; Arber 1925; Rudall 1991); Geissorhiza alone has ligulate leaves. There are water-catching leaves with very distinctive morphologies found especially in taxa from Namaqualand, South Africa (Vogel & Müller-Doblies 2011). For leaf morphogenesis, including the development of plications, see Rudall (1990b).

Genes & Genomes. Moraes et al. (2015) looked at chromosome number evolution in Iridoideae (the numbers are very variable), and also gave some 2C values. Although polyploid species had the highest 2C values, both polyploids and diploids had medium-sized to small genomes. For cytological evolution in Crocus, n = 3<, see Harpke et al. (2013); multiple hybridizations, dysploidy events, and evolution of B chromosomes are all involved.

Chemistry, Morphology, etc. For the occurrence of plumbagin in Aristea, see Harborne and Williams (2001). Homeria and Moraea (Iridoideae) have bufadienolides (cardiac glycosides: Harborne & Williams 2001). Iris contains a greater diversity of isoflavonoids than any other group outside Fabaceae (Reynaud et al. 2005); for xanthones, especially in Iris, see Williams et al. (1997b).

Goldblatt (1990) interpreted the paired "bracts" below the single flowers of Isophysis as representing a reduced rhipidium, a monochasial cymose inflorescence - a rhipidium may then be another synapomorphy for the family. Aristea is palynologically very variable, some members even having disulcate pollen (see Goldblatt & Le Thomas 1997; le Thomas et al. 2001). Crocus has spiraperturate pollen or variants of this, and there is quite substantial infraspecific variation in pollen morphology (Candan & Özhatay 2013 and references: Crocus chrysanthus, also variation in chromosome number). In Sisyrinchium and its relatives the style branches alternate with the stamens; elsewhere the two are usually on the same radius. For a discussion of the caruncles/arils of Iris, see Wilson (2006).

Additional general information is taken from Goldblatt et al. (1998), Goldblatt (2001), and Goldblatt and Manning (2008: generic accounts); see also Mathew (1989) and Crespo et al. (2015), Iris in the old sense and its relatives, Rübsamen-Westenfeld et al. (1994: Geosiris) and Kerndorff et al. (2016: Crocus). For meta carboxy aromatic amino acids, see Larsen et al. 1981), while Rudall et al. (1986) and Rudall (1984: secondary thickening, 1995a) discuss anatomy, Goldblatt et al. (1984) crystals, Wilson (2001) and Steyn (1973a, b), embryology, Cocucci and Vogel (2001) and Rudall et al. (2003a), both nectary evolution, Manning and Goldblatt (1990) endothecial thickenings, Dönmez and Isik (2008) pollen, and Tillich (2003a) seedlings - very variable.

Phylogeny. Iridaceae are monophyletic in nearly all studies (but c.f. Chase et al. 1995a). Initial results suggested that the monotypic Isophysidoideae were sister to the rest of the family, Crocoideae and Iridoideae appeared to be monophyletic, but the status of Aristeoideae was unclear. Reeves et al. (2001a, b: four genes) found that Patersonia, Geosiris, and Aristea were successively sister to a large clade making up [Aristeoideae + Crocoideae]; support was mostly moderate (see also Teixeira de Souza-Chies et al. 1997). If these relationships were confirmed, either the circumscription of Crocoideae would have to be considerably extended, or three more subfamilies would be needed. Goldblatt et al. (2008: five plastid genes) took for this latter option; they found strong support for the pectinations basal to Crocoideae s. str., albeit using successive weighting, which tends to leave one a little uneasy. See Rudall (1994c) for a morphological phylogeny.

Within Iridoideae, the Australian Diplarrhena, whose monosymmetric flowers have only two stamens and pollen grains that are spherical, inaperturate, and intectate pollen, may be sister to the rest (Reeves et al. 2001a, b; Rudall et al. 2003a). The five tribes in Iridioideae are quite well supported and have well-resolved relationships: [Diplarreneae [Irideae [Sisyrincheae [Trimezieae + Tigridieae]]]] (Goldblatt & Manning 2008; also Golblatt et al. 2004, 2006). For diversification of the American Tigridieae, see Rodrigues and Sytsma (2006). Relationships within Trimezieae are being clarified (Lovo et al. 2012). For a phylogeny of Iris, see Tillie et al. (2001) and Wilson (2004); there is phylogenetic resolution of the major groups in the genus (Wilson 2011), although some of the characters used to distinguish groups in the past, such as sepal crests (ridges or more elaborate structures down the midrib of the outer perianth whorl) have turned out to be homoplasious (Guo & Wilson 2014). Wilson et al. (2016) looked at relationships within the royal irises (sect. Oncocyclus). Karst and Wilson (2012) obtained a fair degree of resolution in relationships within New World Sisyrinchium, although species limits there are in a considerable state of disarray (see also Chauveau et al. 2011).

The five tribes of Crocoideae were mostly only moderately supported and their relationships poorly resolved in a study by Goldblatt and Manning (2008; also Goldblatt et al. 2004). Tritoniopsis, with a tubular cotyledonary sheath and tubular cataphyll, may be sister to the rest of the subfamily, but support is at best moderate (Goldblatt et al. 2006; Golblatt & Manning 2008). For a phylogeny of Crocus see Petersen et al. (2008, c.f. in part Frello et al. 2004), and especially Harpke et al. (2013). See Goldblatt and Manning (1998) for a treatment of much of Gladiolus. For relationships within Gladiolus, see Valente et al. (2011, 2012); although there was some resolution towards the base of the tree, many species, especially those from southern Africa, could not be distinguished in these studies.

Classification. I follow the classification suggested by Goldblatt et al. (2008; see also Goldblatt et al. 1998); the subfamilies are for the most part well characterised. See Wilson (2011) for an infrageneric classification of Iris; Crespo et al. (2015) split the genus into twenty five...

[Xeronemataceae [Asphodelaceae [Amaryllidaceae + Asparagaceae]]]: mitochondrial rpl2 gene lost.

Age. Estimates of the age of this node are around (84-)74, 67(-57) m.y. (Bell et al. 2010), ca 100 m.y. (Janssen & Bremer 2004), and (78-)69(-60) or ca 55.8 m.y. (S. Chen et al. 2013).

Phylogeny. This is a strongly supported group in Fay et al. (2000) and Soltis et al. (2007a); see also Janssen and Bremer (2004). The loss of the mitochondrial rpl2 gene occurs either at this node or the next up the tree (see Adams et al. 2002b).

XERONEMATACEAE M. W. Chase, Rudall & Fay   Back to Asparagales


Plant rhizomatous; leaves two-ranked, isobifacial [oriented edge on to the stem]; inflorescence branched, with inflorescence bracts, densely spicate; flowers large; stamens long-exserted, anthers centrifixed; pollen boat-shaped; style solid; ?ovules/carpel; n = 17, 18.

1/2. New Zealand (Poor Knights Island) and New Caledonia.

Chemistry, Morphology, etc. The family is little known, although there is some information in Chase et al. (2000c); the style is scored as if it is hollow in Rudall (2003a).

Previous Relationships. Xeronemataceae were provisionally placed in Asphodelaceae by Takhtajan (1997) and in Hemerocallidaceae by Clifford et al. (1998).

[Asphodelaceae [Amaryllidaceae + Asparagaceae]]: (pedicels articulated); septal nectaries infralocular; ovules with parietal tissue 2-3 cells across.

Age. The age of this node is some (72-)64, 58(-49) m.y. (Bell et al. 2010), ca 93 m.y. (Janssen & Bremer 2004), 75.9 or 81.4 m.y. (Tank et al. 2015: Table S2), 61-54 m.y. (Wikström et al. 2001), (72-)63(-55) or ca 43.6 m.y. (S. Chen et al. 2013), or 67.6 m.y. (Magallón et al. 2015).

Evolution. Divergence & Distribution. For the optimisation of characters like "septal nectaries infralocular" and "ovary superior", see the beginning of this page. The optimisation of successive microsporogenesis on the tree is also uncertain (Chase et al. 2000a); for instance, microsporogenesis varies within Asphodelaceae.

Chemistry, Morphology. Gatin (1920: broad sampling across Liliaceae s.l.) found that taxa that have tepals with single vascular traces are common in this clade, although some have three or more traces; she also studied many other details of pedicel vasculature. Schnarf and Wunderlich (1939) provide embryological details and El-Hamidi (1952) some for the gynoecium from scattered taxa in "Asphodeloideae"; the latter found substantial similarity between all the taxa he examined except Aphyllanthes (Asparagaceae-Aphyllanthoideae). For chromosome sizes of a number of taxa in the group, see Vijayavalli and Mathew (1990 - as Liliaceae).

Phylogeny. This clade has strong support in Fay et al. (2000) and Chase et al. (2000b).

ASPHODELACEAE Jussieu, nom. cons.   Back to Asparagales

Fructan sugars accumulated; (vessel elements in roots with simple perforation plates); styloids +; (stomata paracytic, subsidiary cells with oblique divisions); leaf sheath closed; inflorescence scapose; pedicels articulated; (A not adnate to T); outer integument ³3 cells across, hypostase +; cotyledon not photosynthetic.

41/900. Esp. Old World, not Arctic, western South America.

Age. This crown group is dated to ca 90 m.y. (Janssen & Bremer 2004). Bell et al. (2010), on the other hand, estimate an age of (66-)52, 47(-36) m.y., S. Chen et al. (2013) a variety of ages - (66-)56(-48), ca 47, or ca 39 m.y.a., while (85-)74, 68(-60) m.y. is the age in Crisp et al. (2014), 52.3 m.y.a. in Magallón et al. (2015) and (73/3-)71.3(-69.4) m.y. in McLay and Bayly (2016).

1. Asphodeloideae Burnett


Often rosette-forming leaf succulents, geophytic (rhizomatous) herbs to pachycaul trees, (climbers); monocot secondary thickening widespread; tetrahydroanthracenones + [e.g. chrysophanol]; (velamen +); (monocot secondary thickening +); foliar vascular bundles often inverted, parenchymatous cells in the inner bundle sheath adjacent to the phloem [aloin cells], (sclerenchymatous); leaves spiral or two-ranked, margins often spiny-toothed, (leaf base not sheathing); (inflorescence spicate), (not scapose); (pedicels not articulated), monosymmetry +, ± weak [Haworthia et al.]; T ± free (connate - Kniphofia, etc.), (with a single trace); (anthers centrifixed); microsporogenesis simultaneous; (pollen mixed with raphides); stigma dry (wet); ovules 1-many/carpel, hemitropous, (± straight - Asphodelus clade), outer integument 3-4 cells across, parietal tissue 1 (2) cells across, hypostase +; (capsule fleshy); seed ± angled, aril +, funicular (thin); endosperm thick-walled, hemicellulosic[?], (perisperm +, slight), embryo long; n = (6 - Kniphofia) 7, chromosomes 1.5-20 µm long, usu. bimodal; 3'-rps12 intron lost; (coleoptile +).

Ca 21[list]/785: Aloe (400), Bulbine (75), Kniphofia (70), Trachyandra (50), Eremurus (45), Haworthia (42). Africa, esp. South Africa; also the Mediterranean to Central Asia, Australia, New Zealand (map: see Reynolds 1966; Frankenberg & Klaus 1980; Seberg 2007). [Photo - Collection, Inflorescence, Flowers.]

Age. Crown-group Asphodeloideae are estimated to be (46-)34(-25) or ca 22.5 m.y.o. (S. Chen et al. 2013) or (75-)69-58(-51) m.y.o. (Crisp et al. 2014: see discussion after Xanthorrhoeoideae, the two models not differing here).

Synonymy: Aloaceae Batsch

[Xanthorrhoeoideae + Hemerocallidoideae]: anthraquinones +; raphides 0.

Age. The age of this node is (63-)52.5(-45) or ca 46.4 m.y. in S. Chen et al. (2013) or rather older, (71.2-)67.1(-62.5) m.y., in McLay and Bayly (2016). Note that the age of Xanthorrhoea stem in Crisp et al. (2014) is based on the topology [Hemerocallidoideae [Xanthorrhoeoideae + Asphodeloideae]].

The 47.8-38 m.y.o. fossil Dianellophyllum eocenicum from Central Australia has been placed at the stem node of Hemerocallidoideae (Iles et al. 2015).

2. Xanthorrhoeoideae M. W. Chase, Reveal & M. F. Fay


Stem thick, woody, erect (not); monocot secondary thickening +; plant resiniferous; ?vessels; layer of sclerenchyma below epidermis in leaves; stomata paracytic; leaves spiral, unifacial, leaf base not sheathing; inflorescence densely spike-like, branches cymose, congested; flowers sessile, not articulated; T = 3 dry + 3 subpetal-like, free; stamens long exserted; microsporogenesis successive [tetrads tetragonal]; pollen extended sulcate; stigma ± punctate, ?wet; ovules several/carpel, outer integument ca 3 cells across, apex of nucellus pointed, hypostase?; inner cuticle of tegmen +; seeds flattened; endosperm quite thick-walled, development?, little hemicellulose, embryo transverse to long axis of seed; n = 11, (bimodal); hypocotyl short.

1[list]/30. Australia (map: from Australia's Virtual Herbarium, i.2015). [Photo - Habitat, - Habit, Inflorescence.]

Age. Crown-group Xanthorrhoeoideae are estimated to be a mere (3.8-)1.7(-0.3) m.y.o. (S. Chen et al. 2013) or (59-)35-24(-13) m.y. (Crisp et al. 2014), although the latter also obtained some very young ages, most in the range of (13-)6.4, 3.3(-1.8) m.y.a., one somewhat older. Crisp et al. (2014) preferred the older (first) estimates, which came from using a random local clocks model, over the younger ages, which came from an uncorrelated lognormal relaxed clock model; the latter, they thought, could not handle the substitution rate changes.

Synonymy: Xanthorrhoeaceae Dumortier, nom. cons.

3. Hemerocallidoideae Lindley


Habit various; flavonols, naphthoquinones, saponins +; roots often swollen; (vessels in the stem); mucilage cells 0; cuticular wax rodlets parallel; leaves (spirally) two-ranked, vernation conduplicate to flat-conduplicate or plicate, (semi-ensiform, isobifacial); (inflorescence not scapose); (bracteoles lateral), (flowers monosymmetric); (median tepal of outer whorl adaxial - Hemerocallis), T tube short (1/2 way - Hemerocallis; 0); filaments often ornamented/swollen, (anthers (centrifixed), dehiscing by pores - Dianella and relatives); microsporogenesis simultaneous (successive), pollen trichotomosulcate (tetrachotomosulcate, monosulcate), usu. <30µm across, pollenkitt +; stigma dry (wet), (3-parted - Pasithea); ovules 1-many/carpel, outer integument 6-7 cells across, inner integument 2-4 cells across, parietal tissue none, nucellar cap ca 2 cells across (0), podium well developed, hypostase 0; antipodal cells large, persistent; fruit also a berry (nut); seeds ovoid, (flattened - Phormium), (with strophiole/aril - Johnsonia et al.); endosperm hemicellulosic, usu. helobial, embryo not central [Geitonoplesium], also short; n = 4 [Agrostocrinum], 8, 9, 11, 12, chromosomes 0.8-17.33 µm long; (cotyledon not photosynthetic - Dianella), epicotyl long or not, (hypocotyl 0; collar +), primary root well developed, branched or not.

20[list]/89: Dianella (20-40). Papuasia to New Zealand and the Pacific, esp. Australia (e.g. all 8 genera of Johnsonieae s. str.), also Europe to Asia, Malesia, India, Madagascar, Africa; two genera and two species in South America (map: from Fl. Austral., Wurdack & Dorr 2009). [Photo - Habit, Flower, Flower].

Age. Crown-group Hemerocallidoideae are (53-)45(-36) or ca 39 m.y.o. (S. Chen et al. 2013) or (63.6-)58(-52.4) m.y. (McLay & Bayly 2016).

Synonymy: Dianellaceae Salisbury, Eccremidaceae Doweld, Geitonoplesiaceae Conran, Hemerocallidaceae R. Brown, Johnsoniaceae J. T. Lotsy, Phormiaceae J. Agardh

Evolution. Divergence & Distribution. For additional divergence dates within Hemerocallidoideae, see McLay and Bayly (2016). The subfamily is Australian with the exception of the Eurasian Simethis and Hemerocallis, which makes things biogeographically interesting (McLay & Bayly 2016).

Asphodelaceae-Asphodeloideae are very diverse (ca 340 species) in southern Africa (Johnson 2010). Eccremis and Pasithea represent independent migrations of the phormioid clade to South America (Wurdack & Door 2009), while Bulbinella (Asphodeloideae) grows in South Africa and New Zealand.

For an ecological account of Xanthorrhoea, see Lamont et al. (2004); some diversification in the genus may be associated with the aridification of the Nullarbor Plain some 14-13 m.y.a. that separated eastern and western clades (Crisp & Cook 2007).

Pollination Biology & Seed Dispersal. Many species of the large genus Aloe (Asphodeloideae), perhaps some 85 species in southern Africa alone, are pollinated by birds (Rebelo 1987), short-billed birds other than typical nectar-eaters visiting some species with dark-coloured and bitter-tasting nectar that are not deterred by its taste (Johnson et al. 2006). There is also insect pollination, perhaps especially among the short-tubed species (Symes et al. 2009; Hargreaves et al. 2008, 2012), as in other groups of Asphodelaceae. Buzz pollination probably predominates in Hemerocallidoideae, and the small pollen (but c.f. Arnocrinum and Hemerocallis itself), although not the presence of pollenkitt, is consistent with this (Furness et al. 2014)

A number of Hemerocallidoideae have myrmecochorous seeds (Lengyel et al. 2010).

Vegetative Variation. Most members of the phormioid clade (Hemerocallidoideae) have leaves that are more or less isobifacial immediately above the sheath, but higher up they become dorsiventrally flattened and more "normal" in appearance; Pasithea, sister to the rest of the clade, lacks this isobifacial zone (Wurdack & Dorr 2009). Members of Asphodeloideae have more or less succulent leaves, and species of Aloe and Haworthia in particular are commonly rosette plants with massively fleshy leaves; these can be borne in spirals or be distinctively two-ranked. As with Aizoaceae from southern Africa, there is great variation in the micromorphology of their epidermis (Cutler 1982); the two grow in similar extreme habitats. For the remarkable water-catching leaves in taxa growing in foggy deserts in Namaqualand, South Africa, see Vogel and Müller-Doblies (2011). Geitonoplesium (Hemerocallidoideae) has resupinate leaves.

Chemistry, Morphology, etc. The old Alooideae (= Asphodeloideae, part) are chemically very distinctive (Klopper et al. 2010 for a summary). Aloin, an anthraquinone glycoside, is a laxative commonly found in Aloe. These old Alooideae have 1-methyl-8-hydroxyanthraquinones, e.g. chrysophanol, in the roots and anthrone-C-glycosides in the leaves (e.g. Manning et al. 2014). In Asphodeloideae Bulbine, Trachyandra, and Kniphofia all have knipholone, an anthraquinone derivative (van Wyck et al. 2005), but it appears not to have been reported from the Asphodelus clade. Johnsonia (Hemerocallidoideae) has chelidonic acid (Ramstad 1953).

The apical meristem of the stem in Xanthorrhoea media is massive - 580-1283 µm across (Staff 1968, q.v. for details of stem growth). The sieve tube plastids of the Aloe group also have peripheral fibres in addition to the central protein crystal. Aloin cells are reported from Dianella (Hemerocallidoideae: see Rudall 2003a); on the other hand, Kniphofia lacks aloin cells, having a well developed sclerenchymatous cap in their place (as have some other Asphodelaceae, even some Alooideae). It is unclear if aloin cells are secretory (Beaumont et al. 1985: survey and chemistry). The vascular bundles in the leaf form a circle and there are globules in the outer bundle sheath (also in Kniphofia); the central cells of the leaf are gelatinous. The old Aloideae are reported to have tetracytic stomata (e.g. Cutler 1972), although this is questioned by G. Smith and van Wyk (1992).

The inflorescences of Xanthorrhoea are described as being terminal (Clifford 1998); they are sometimes axillary in Asphodeloideae. Within Hemerocallidoideae Hemerocallis itself seems to have lateral bracteoles, as does Dianella; both may have "inverted" flowers (e.g. Eichler 1875; Ehrhardt 1992), although in Hemerocallis, at least, this seems to be variable. Hemerocallis flowers with the median outer tepal adaxial are common, but the seal of the Daylily Society shows a flower with the normal monocot orientation! The number of vascular bundles supplying the tepals in members of this subfamily varies from (1-)3-9(-25) (Clifford et al. 1998a) and the stamens are often rather elaborate. In at least some species of Aloe the larger stamens are opposite the inner whorl of tepals.

Both Hemerocallidoideae and Xanthorrhoeoideae have ovaries that can be interpreted as being secondarily superior and that have infra-locular septal nectaries (Rudall 2002, 2003a). Ovule orientation at the basal node in the family is unclear (c.f. Steyn & Smith 1998). Kniphofia has a bistomal micropyle and a nucellar endothelium (Takhtajan 1985). Daru et al. (2013) noted that seedlings of Aloe and Gasteria have two-ranked leaves, whatever the leaf arrangement in the adults.

Microsporogenesis in Hemerocallis was described as being successive and the endosperm as being nuclear by Di Fulvio and Cave (1965, but c.f. Cave 1955). Hemerocallis also has isoflavones, monosulcate pollen and a wet stigma, but it lacks a nucellar cap and septal nectaries. In pollen morphology Hemerocallis was considered to be derived by Chase et al. (1996); with Simethis, which has trichotomosulcate pollen, it is sister to the rest of Hemerocallidoideae (see also McPherson et al. 2004; Wurdack & Dorr 2009; Furness et al. 2014 - is microsporogenesis in the latter known?); monosulcate pollen in Hemerocallidoideae then represents a reversal. Given that Chamaescilla also has monosulcate pollen, the story becomes more complicated (McLay & Bayly 2016).

For general information, see G. Smith and Van Wyk (1998), Clifford and Conran (1998: Johnsoniaceae), Clifford et al. (1998a) and Reynolds (1966, 2004) and Carter et al. (2011), esp. Aloe, well illustrated, see also Riley and Majumdar (1979: biosystematics), Van Wyk et al. (1995, 2005) and Grace et al. (2010:), all chemotaxonomy, Kite et al. (2000: anthroquinones), G. Smith et al. (1992: anatomy), Ely and Luque Arias (2006: anatomy of Eccremis), Kosenko (1994: pollen of Phormium), Furness et al. (2014: pollen of Hemerocallidoideae), Shamrov (2014a: gynoecium of Hemerocallis), Cave (1955, 1975), Raju (1957), Berg (1962) and di Fulvio and Cave (1965), all embryology, Steyn and Smith (1998: ovule morphology, 2001) and Thadeo et al. (2015: fruit anatomy).

For Xanthorrhoea, some information is taken from Chanda and Ghosh (1976: pollen), Rudall (1994b: embryology), Rudall and Chase (1996: phylogeny) and Bedford et al. (1986) and Clifford (1998), both general.

Phylogeny. There is strong support for Asphodelaceae s.l. (in much recent literature the name used has been Xanthorrhoeaceae s.l.) in Fay et al. (2000), Wurdack and Dorr (2009), etc. However, relationships within the clade were initially unclear. There is slight support for a [Xanthorrhoeoideae + Asphodeloideae] clade in the three-gene tree of Chase et al. (2000a; see also Fay et al. 2000; Crisp et al. 2014: chloroplast genes); some analyses in Chase et al. (2000a) also suggested an [Asphodeloideae + Hemerocallidoideae] clade. Hemerocallidoideae, and perhaps also Asphodeloideae, were paraphyletic in a rpb2 analysis of Crisp et al. (2014: ?rooting). However, Devey et al. (2006) found support for a [Xanthorrhoeoideae + Hemerocallidoideae] clade (see also Pires et al. 2006; Graham et al. 2006; Wurdack & Dorr 2009: good-moderate support; Seberg et al. 2012; Steele et al. 2012: strong support; Hertweck et al. 2015; S. Chen et al. 2013). Rudall (2003a) suggested that there were close morphological relationships between Hemerocallidaceae and Asphodelaceae - and between Xanthorrhoeaceae and Iridaceae...

Within Asphodeloideae, Aloe and its immediate relatives (= Alooideae s. str.: Klopper et al. 2010 for a summary) seem distinct and form a monophyletic group. However, more ordinary-looking Bulbine is sister to this clade, and then come other Asphodeloideae, including Kniphofia et al. and Eremurus et al., which together form a clade (Naderi Safar et al. 2014); an [Asphodelus + Asphodeline] clade (n = 14) is sister to the rest of the subfamily, and with good support (see Devey et al. 2006 for a phylogeny, inc. details of that of Bulbine, also references below; McLay and Bayly 2016). Ramdhani et al. (2009) discussed the phylogeny of Kniphofia. Some species of Bulbine have a bimodal karyotype of n = 7, 4 long and 3 short (Spies & Hardy 1983), rather like the karyotype of Aloeae (4L + 3S: Chase et al. 2000a; Devey et al. 2006; Pires et al. 2006); they probably evolved independently, but they also have similar medicinal properties... For relationships around Aloe, which remained poorly understood and little resolved for some time, see Treutlein et al. (2003a, b), and for those around Haworthia, see Ramdhani et al. (2011). Daru et al. (2013) and in particular Manning et al. (2014) have clarified relationships there, although support for some of the basal branches could be improved, and both Aloe and Haworthia are scattered through the tree.

There are two well supported clades within Hemerocallidoideae, the phormioid and [hemerocalloid + johnsonioid] clades (e.g. Wurdack & Dorr 2009; also Seberg et al. 2012; Crisp et al. 2014). The loss of the 3'-rps12 intron characterises the [hemerocalloid + johnsonioid] clade (= [Johnsonieae [Hemerocallis + Simethis]]), see McPherson et al. (2004) and Chase et al. (2000b). Chamaescilla (ex Asparagaceae-Lomandroideae) has recently been found to be sister to the [Hemerocallis + Simethis] clade (McLay & Bayly 2016). Pasithea, from South America, is sister to all other phormioids (Wurdack & Dorr 2009; Seberg et al. 2012; Crisp et al. 2014), while the other New World genus, Eccremis, previously of uncertain relationships (e.g. Clifford et al. 1998a) because of interpretations of morphology, is sister to Dianella (Wurdack & Dorr 2009); these relationships were also recovered by McLay and Bayly (2016).

Classification. A.P.G. II (2003) suggested as an option the inclusion of Asphodelaceae, Xanthorrhoeaceae and Hemerocallidaceae in Xanthorrhoeaceae s.l., and this circumscription was adopted by A.P.G. III (2009), but because of nomenclatural issues the name has been changed to Asphodelaceae (A.P.G. IV 2016), otherwise, see Chase et al. (2009b). The recognition of an Alooideae (= Asphodeloideae-Aloeae) would make Asphodeloideae paraphyletic and necessitate the recognition of several other subfamilies.

G. Smith and Steyn (2004) discuss the taxonomy of Alooideae; generic limits around Aloe are decidedly unsatisfactory. However, Grace et al. (2013) and in particular Manning et al. (2014) have revised the classification of the whole group, recognising 11 genera.

Species limits are problematic in Aloe, in Kniphofia (Ramdhani et al. 2009), and in Haworthia (Ramdhani et al. 2011: ?hybridization; Bayer 2009: some comments and references), both Alooideae. Species estimates in Dianella (Hemerocallidoideae) range from 25-350+ (Carr 2007).

Thanks. I thank Syd Ramdhani and Matt Ogburn for useful discussions.

Previous Relationships. Three genera that used to be placed in Asphodelaceae s. str., i.e. in Asphodelaceae-Asphodeloideae, are now in Hemerocallidoideae (Simethis), Asparagaceae-Asparagoideae (Hemiphylacus), and Asparagaceae-Agavoideae (Paradisea, Anthericaceae s. str.) respectively, while Chamaescilla has moved to Asphodelaceae-Hemerocallidoideae from Asparagaceae-Lomandroideae- the evidence is largely molecular (Chase et al. 2000b; McLay & Bayly 2016).

[Amaryllidaceae + Asparagaceae]: microsporogenesis successive [possible place]; endosperm development?

Age. This node is ca 91 m.y.o. (Janssen & Bremer 2004), ca 71.5 m.y.o. (Tank et al. 2015: Table S2), 58-51 m.y.o. (Wikström et al. 2001), (69-)60, 54(-45) m.y. (Bell et al. 2010), (67-)41(-50) or ca 41.6/40.6 m.y. (S. Chen et al. 2013), or about 62.5 m.y. (Magallón et al. 2015).

Chemistry, Morphology, etc. Where do steroidal saponins occur in this clade? Microsporogenesis is uniform here. In other Asparagales with successive microsporogenesis, details of wall formation (centrifugal cell plates) is similar to those members of this clade that have been studied, however, plate formation may also be centripetal when microsporogensis is simultaneous (Nadot et al. 2006). For chromosome size in Liliaceae s.l. and relatives, i.e. some taxa in this area, see Vijayavalli and Mathew (1990).

Phylogeny. This is a strongly supported clade (e.g. Chase et al. 1995a; Fay et al. 2000; Chase et al. 2000b; Graham et al. 2005), however, inclusion of Aphyllanthes in analyses has tended to decrease support for the clades within it (Graham et al. 2006). Kim et al. (2011: seven genes, three compartments) found that Amaryllidaceae grouped with Asparagoideae, Lomandroideae and Nolinoideae; other members of this clade formed a separate group.

AMARYLLIDACEAE J. Saint-Hilaire, nom. cons.   Back to Asparagales

Fructan sugars accumulated; leaves two-ranked; inflorescence scapose, umbellate, cymose, inflorescence bracts 2 or more, scarious, internal bracts small; pedicels not articulated; flowers large [>1.5 cm long and across]; (T free); (A connate basally); style long, stigma dry; parietal tissue none; endosperm nuclear or helobial; hypocotyl 0.

73/1605. Worldwide - three subfamilies below.

Age. Estimates of the age of crown-group Amaryllidaceae are ca 87 m.y.o. (Janssen & Bremer 2004) and (62-)51(-42) or ca 33.7 m.y.o. (S. Chen et al. 2013).

Bacterial/Fungal Associates. Fungi on Allium and other Allioideae are rather different from those on Amaryllidoideae (e.g. Savile 1962).

Chemistry, Morphology, etc. Distinctive, mannose-binding lectins (the specificity is absolute) are found in Allioideae and Amaryllidoideae (van Damme et al. 1991: known from Agapanthus?). Very large genomes with a C value of some 350 picograms or more are found in some Amaryllidaceae-Allioideae and -Amaryllidoideae - also in Asparagaceae-Scilloideae (Leitch et al. 2005). For tapetal cells, see Wunderlich (1954), for inflorescence structure, see Weberling (1989).

Phylogeny. This is a very strongly supported clade (e.g. Fay et al. 2000, but c.f. McPherson et al. 2004; Thomas et al. 2005), and it has some characters! Meerow et al. (1999), Fay et al. (2000: strong support), Givnish et al. (2006), Pires et al. (2006) and Seberg et al. (2012: support weak) suggest a set of relationships [Agapanthaceae [Alliaceae + Amaryllidaceae]], although Meerow et al. (2000a) found Agapanthaceae to be sister to Amaryllidaceae, albeit with weak support.

Classification. Combining the three families Agapanthaceae, Alliaceae and Amaryllidaceae into Alliaceae s.l. was an option in A.P.G. II (2003), an option that was exercised in A.P.G. III (2009), although under the name of Amaryllidaceae. The infrafamial classification follows that in Chase et al. (2009b).

1. Agapanthoideae Endlicher Agapanthoideae

Plant rhizomatous; velamen +; laticifers +?; leaf vernation flat; inflorescence bracts connate along one side, other bracts?; flowers weakly monosymmetric; T ± connate basally; anther middle layer of wall from outer secondary parietal cells; ovules apotropous; seeds flat, winged; endosperm with starch/hemicellulose, embryo short; n = (14) 15 (16), chromosomes 4-9 µm long; seedling as in Allioideae?

1/9. South Africa (map: from Leighton 1965). [Photo - Habit, Flower.]

Chemistry, Morphology, etc. Information is taken from Kubitzki (1998b: general); D. Zhang et al. (2010) describe sporogenesis and gametogenesis (there are reports of occasional embryos with two cotyledons), and Zhang et al. (2011) embryogeny.

Synonymy: Agapanthaceae F. Voigt

[Allioideae + Amaryllidoideae]: plants geophytes, bulbous, tunicate, with contractile roots; lectins binding mannose; (corona +); (embryo sac bisporic, eight nucleate - Allium type).

Age. The age of this node is estimated at (62-)50, 46(-35) m.y. by Bell et al. (2010) and at (56.5-)47(-38) or ca 30.3. m.y. by S. Chen et al. (2013).

2. Allioideae Herbert

Flavonoids, cysteine-derived sulphur compounds +; raphides often 0, styloids +; laticifers +; leaves (spiral), sheath closed, long, shortly ligulate [Allium, at least]; flowers medium sized [<1 cm long, <1.5 cm across]; T ± connate; A connate or adnate to free; style solid, (stigma wet); ovules 2-many carpel, in two ranks, campylotropous (anatropous), (micropyle bistomal), nucellar cap +/0, obturator +; seeds angular, exotestal, other layers of testa collapsed or not; (endosperm pitted); chromosomes 2-20 µm long; (cotyledon not photosynthetic).

13[list]/795. Mainly South America, but Allium esp. N. Temperate Eurasia - three groups below. [Photo - Collection] [Photo - Inflorescence, Flower, Flower.]

Age. Crown-group Allioideae are estimated to be (44.5-)37(-28) or ca 30.3 m.y.o. (S. Chen et al. 2013).

2A. Allieae Dumortier


Bulbs lacking starch, (plant ± rhizomatous); vessel elements in roots often with simple perforation plates; leaves ± unifacial; T basally connate, with one trace; A both basally connate and adnate to C, filaments often winged, at least basally, tapetal cells uninuclear; (G semi-inferior), style ± gynobasic, (paired projections from the ovary); ovules 2-14/carpel, epi- or apotropous, outer integument 4-6 cells across, inner integument ca 3 cells across; embryo sac bisporic, eight nucleate [Allium type]; (seed with caruncle); endosperm cellular, embryo long, curved; n = (7) 8 (9-11), chromosomes 9.0-19.3 µm long, TTAGGGn [human-type] telomeric repeats lost.

1/260-850. North temperate, often seasonally dry, especially the Mediterranean to Central Asia, west North America, scattered in Africa (map: from Hultén 1962; de Wilde-Duyfjes 1976; Hanelt 1990; Hanelt et al. 1992; Fl. N. Am. 26: 2002, not native in Iceland).

Synonymy: Alliaceae Borkhausen, nom. cons., Cepaceae Salisbury, Milulaceae Traub


[Tulbaghieae + Gilliesieae]: bulbs with starch; corona +; endosperm helobial; embryo short.

2B. Tulbaghieae Meisner

Plant rhizomatous; leaf sheath short; flowers bracteate; T rather strongly connate, corona massive, 3-lobed, lobes connate or not [opposite inner T]; A sessile, adnate to corolla tube and/or corona; ovules 2-several/carpel; seeds ± flattened; n = 6, chromosomes 11.5-14.7 µm long.

1/22. Southern Africa (map: from Vosa 1975; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012).

Synonymy: Tulbaghiaceae Salisbury


2C. Gilliesieae Baker

(Sulphur compounds ?0 - plant not smelling); (flowers monosymmetric); (T 3), (3 + 3 reduced); corona + [of a few to several linear structures, often 3 opposite inner T]/0; A (2), (3, opposite outer T), (variously connate and adnate), (extrorse), (staminodes +); ovules 2-many/carpel, style solid [Nothoscordum], stigma ± punctate to 3-lobed; (ovule with inner integument 5-7 cells across - Dichelostemma); (embryo sac bisporic, eight nucleate [Allium type]); n = 4-10, 12, etc., chromosomes 17-30 µm long.

10/80: Nothoscordum (25). South U.S.A., Mexico to South America (map: from Fl. North America 26. 2002).

Synonymy: Gilliesiaceae Lindley

Evolution. Divergence & Distribution. Nguyen et al. (2008) found that Old and New Word species of Allium are mostly in two separate clades, although basal to the clade containing all North American members (in subgenus Amerallium) are Eurasian taxa. Diversity within North America Allium is centred in the west, especially in California, and a number of species there are serpentine endemics (Nguyen et al. 2008).

Pollination Biology & Seed Dispersal. Gilliesia has very strongly monosymmetric flowers with only two stamens; the flowers may mimic insects (Rudall et al. 2002). For septal nectaries and where nectar ends up in the flower, see Vogel (1998b).

Vegetative Variation. The apparently bifacial leaves of at least some species of Allium have inverted vascular bundles along the adaxial surface and vascular bundles with normal orientation along the abaxial surface (Mathew 1996). In a comprehensive study, Mashayekhi and Columbus (2014) looked at the leaf anatomy of 67 species of Allium, i.a. species with terete, unifacial leaves might have a ring of bundles or a single series of normally oriented bundles, and species with flattened leaves sometimes had two series of normally-oriented bundles.

Genes & Genomes. There has been a major movement of ribosomal protein and succinate dehydrogenase genes from the mitochondrion in Allium (Adams & Palmer 2003). Allium has also lost its TTAGGGn telomere minisatellite terminal sequence repeats, and although some species do have this repeat, it is not telomeric (Sýkorová et al. 2006a).

Chemistry, Morphology, etc. The flowers of Allium are shown with the median member of the outer whorl in the adaxial position (Spichiger et al. 2004). Schickendantziella (Gilliesieae) has only three tepals; they are caudate. Coronal structures in Gilliesieae vary in number and are often more or less linear; they may be staminodial in some species (ref.?), but this is unlikely since the number of stamens + linear processes usually = >6, and taxa with more than six stamens are uncommon in this part of the tree. Do all Allioideae have apotropous ovules?

Some information is taken from Rahn (1998: general), and Sundar Rao (1940), Berg (1996) and Berg and Maze (1966), all embryology. For Allium, see Rabinowitch and Currah (2002: more horti-/agricultural), Fritsch and Friesen (2002 [and many other papers in same book]: general), Fritsch and Keusgen (2006: cysteine sulphoxide distribution), Choi et al. (2011: floral development, esp. epidermis), Messeri (1931: cytology and embryology). See also Vosa (1975), cytology and revision of Tulbaghia.

Phylogeny. Fay and Chase (1996) discuss relationships within the subfamily; the topology is [Allieae [Tulbaghieae + Gilliesieae]], although the support for the clades is rather weak. Fay et al. (2006b) found that part of Ipheion was embedded in Nothoscordum; for relationships around Leucocoryne, see Souza et al. (2015). Nguyen et al. (2008) provide a phylogeny for Allium, in which there are three main clades (see also Friesen et al. 2006; Hirschegger et al. 2010: section Allium; Huang et al. 2014); the relationships of members of the small subgenera Nectaroscordum and Microscordum are unclear (Nguyen et al. 2008; Mashayekhi & Columbus 2014). For relationships in subgenus Amerallium, which includes nearly all North American species, see Choi et al. (2012), Li et al. (2012, and Mashayekhi and Columbus (2014: most sections not monophyletic). In the large subgenus Melanocrommyum of Allium there seems to be extended incomplete lineage sorting, and morphological sections are not supported by molecular data (Gurushidze et al. 2008, esp. 2010).

Classification. See Fay and Chase (1996: as Alliaceae). Friesen et al. (2006) provide a subgeneric and sectional classification of Allium which has since been elaborated (see above); Gregory et al. (1998) list names included in it.

3. Amaryllidoideae Burnett   Back to Asparagales


Norbelladine alkaloids, non-protein amino acids, chelidonic acid +, saponins 0; (velamen +, 2-4-layered); sclerechymatous ring in scape, bundles in rings; petiole bundles in arc; (lacunae formed by breakdown of parenchyma); leaves (spiral), vernation flat or revolute to involute, (vascular bundles inverted; base sheathing); bracts equitant[?]; flowers large, (monosymmetric), median member of outer tepalline whorl adaxial; T ± free, corona +/0 [morphology various]; anther middle layer of wall from outer secondary parietal cells; (tapetal cells uninucleate); ovary inferior, stigma capitate to deeply trifid, (wet); (ovule with outer integument ³3 cells across), (inner integument o 4 cells across), (nucellar cap ca 2 cells across); endosperm starchy or with hemicellulose (thin-walled), embryo poorly differentiated, small; n = (5-)11(12<), chromosomes (1.5-)3-28 µm long; cotyledon bifacial, (not photosynthetic), primary root well developed, contractile.

59[list]/800+ - fourteen groups below. Tropical (temperate), esp. South America and Africa, also Mediterranean (map: from Allan Meerow and O. Seberg, pers. comm.; Snijman 1984; Fl. N. Am. 26: 2002; de Castro et al. 2012). [Photo - Flower, Fruit.]

Age. Crown-group Amaryllidoideae are (39-)28.5(-19) or ca 15.9 m.y.o. (S. Chen et al. 2013).

3A. Amaryllideae Dumortier

(Growth monopodial - Crinum); stomata paracytic, subsidiary cells with oblique divisions; extensible [helically-thickened] fibres in leaf; leaves follow the flowers, (perennial - many Crininae); corona + [of webbing joining filaments basally, or small appendages developed from filaments], or 0 [Crinineae]; tectal cells binucleat; pollen bisulcate, exine gemmate, with scattered spinules, intectate-columellate; (style laterally displaced); ovules unitegmic (ategmic - Crinum); embryo sac bisporic and 8-celled [Allium type], (antipodal cells persistent); seeds water-rich, non-dormant, phytomelan 0, testa to 25 cells thick, chlorophyllous, with stomata, or ± collapsed, (0, cork layer in endosperm - Crinum); endosperm chlorophyllous, usu. with a corky layer, starchy, embryo chlorophyllous; (n = 10, 12, 15), chromosomes 5.3-20.5 µm long.

11/146: Crinum (65), Strumaria (23). SubSaharan, especially South Africa, Crinum Pantropical.

Synonymy: Crinaceae Vest, Strumariaceae Salisbury

Calostemmateae, etc.: bundle sheath cells parenchymatous.

[Calostemmateae [Cyrtantheae + Haemantheae]]: ?

3B. Calostemmateae D. & U. Müller-Doblies

Ovules 2-3/carpel; embryo germinates precociously producing a bulbil; fruit dry, indehiscent; phytomelan 0; n = 10, chromosomes 3.3-8 µm long.

2/4. Australia, Malesia.

[Cyrtantheae + Haemantheae]: scape lacking sclerenchymatous ring, subepidermal collenchyma +; 1-layered rhizodermis +, velamen 0; fruit indehiscent.

3C. Cyrtantheae Traub

Seeds flat, winged, horizontally stacked, phytomelan +; n = (7) 8 (11).

1/50 (Cyrtanthus). Africa, especially the south.

Synonymy: Cyrtanthaceae Salisbury

3D. Haemantheae Hutchinson

(Plant rhizomatous); (alkaloids 0 - Gethyllis); inflorescence bracts connate, (flowers single - Gethyllis, etc.); (A 12); fruit baccate; seeds angled, etc.; phytomelan 0 (+); n = 6, 8, 9, 11, 12; chromosomes 3.0-24 µm long.

6/80: Gethyllis (32), Haemanthus (22). Tropical Africa, mostly in the South.

Synonymy: Gethyllidaceae Rafinesque, Haemanthaceae Salisbury

[[Lycoridae [Galantheae, Pancratieae, Narcisseae]] [Hippeastreae [Eustephieae [Hymenocallideae, Stenomesseae, Eucharideae]]]]: ?

[Lycoridae [Galantheae, Pancratieae, Narcisseae]] / Eurasian Clade: seeds subglobose, turgid.

3E. Lycoridae D. & U. Müller-Doblies

(Seeds irregularly discoid - Ungernia); n = 11 (etc.).

2/26: Lycoris (20). Temperate to subtropical East Asia to Iran.

[Galantheae, Pancratieae, Narcisseae]: ?

3F. Galantheae Parlatore

(Roots not medullated); (inflorescence bracts connate along one side); (anthers dehiscing by pores); elaiosome + (0); n = 7-9, 11, 12.

8/31: Galanthus (17). Europe to N. Africa, the Crimea and the Caucasus.

Synonymy: Galanthaceae G. Meyer, Leucojaceae Borkhausen

3G. Pancratieae Dumortier

Corona + [filaments joined by toothed tube]; n = 11, chromosomes 8.7-22 µm long.

1/20. Mediterranean, southern Asia, to sub-Saharan Africa.

Synonymy: Pancratiaceae Horaninow

3H. Narcisseae Lamarck & de Candolle

(Roots not medullated); inflorescence bracts basally connate; (corona + [tubular, from tepals - Narcissus]); parietal tissue to 2 cells across; elaiosome + (0); n = (7) 11 (13), etc.

2/58: Narcissus (50). Europe to W. Asia and N. Africa.

Synonymy: Narcissaceae Jussieu

[Hippeastreae [Eustephieae [Hymenocallideae, Stenomesseae, Eucharideae]]] / Andean + Extra-Andean/American Clade: 1-layered rhizodermis +, velamen 0; scape lacking sclerenchymatous ring, subepidermal collenchyma +; bracts obvolute; (seeds flat, horizontally stacked), phytomelan common.

3I. Hippeastreae Sweet

Inflorescence bracts often connate basally (along one side) or not; flowers (very strongly) monosymmetric (polysymmetric); T tube short to long, (corona +); A declinate, of varying lengths (not declinate); stigma capitate to 3-lobed; seeds flattened, winged or D-shaped; n = 6-13, 17, etc., chromosomes 3-16.7 µm long.

11/218: Hippeastrum (55), Zephyranthes (50), Habranthus (50). S.E./S.W. U.S.A., the Caribbean, and Central and South America.

Synonymy: Brunsvigiaceae Horaninow, Oporanthaceae Salisbury, Zephyranthaceae Salisbury

[Eustephieae [Hymenocallideae, Stenomesseae, Eucharideae]] / Andean Tetraploid Clade: palisade leaf mesophyll absent; flowers polysymmetric; x = 23 [tetraploid].

3J. Eustephieae Hutchinson

A of two lengths; seeds flattened, winged; (n = 21, etc.).

3/15: C. Andes (Peru, Bolivia, Argentina).

[Hymenocallideae, Stenomesseae, Eucharideae]: ?

3K. Hymenocallideae Small

Pollen grains with the ends narrowed, with different sculpture [auriculate]; testa thick, spongy, chlorophyllous, vascularized, phytomelan 0 (+ - Leptochiton); embryo starchy; (n = 19, 20, 22), chromosomes 4-11.8 µm long.

3/65: Hymenocallis (50). S.E. U.S.A., the Antilles, Central America to Bolivia.

3L. Stenomesseae Traub

(Velamen + - Pamianthe); leaves petiolate, strap-shaped; staminal cup + (0); seeds flattened, obliquely winged.

8/62: Stenomesson (35). Costa Rica (1 sp.), Andean South America S. to Bolivia.

3M. Eucharidae Hutchinson

Leaves petiolate, elliptic; (flowers monosymmetric); seeds globose, turgid, coat lustrous; chromosomes 2.3-10.7 µm long.

4/28: Eucharis (17). Central America, the Andes S. to Bolivia.

Evolution. Divergence & Distribution. Meerow (2010) discussed diversification in American Amaryllidaceae in terms of the interplay of canalization and genome doubling, emphasizing the floral and vegetative diversity encompassed by the Andean tetraploid-derived clade. Santos-Gally et al. (2012) discussed the biogeography of the Mediterranean-centred Narcissus. About a third of the subfamily, ca 280 species, grow in southern Africa (Johnson 2010).

Petiolate leaves have evolved at least six times in the family (?ref).

Ecology & Physiology. Amaryllidoideae are an important component of the distinctive Cape geophytic flora (Procheŝ et al. 2006) having about 100 species endemic there. For water-catching leaves with very distinctive morphologies that are found especially in taxa from Namaqualand, South Africa, see Vogel and Müller-Doblies (2011).

Pollination Biology & Seed Dispersal. Monosymmetry is said to be ancestral in the subfamily (Meerow & Snijman 1998; Meerow 2010). It is certainly very labile, reversals and parallelisms being common, and it is perhaps under simple genetic control (Meerow et al. 1999). Some kind of corona is common, but its morphological nature varies (see below). The flowers are protandrous. A number of species of Amaryllis are heterostylous (Santos-Gally 2013 and references).

Bird pollination is quite important in Amaryllidaceae. A. Meerow (pers. comm. ii.2014) estimated that around 100-150 species of South American Amaryllidaceae (genera like Brunswigia, Hippeastrum, Stenomesson) may be pollinated by humming birds, while in southern Africa ca 13 species of Cyrtanthus alone are pollinated by sunbirds (Snijman & Meerow 2010) - several other kinds of pollinators service that genus.

Almost three hundred species in the subfamily have myrmecochorous seeds (Lengyel et al. 2010). Wind dispersal of the seed is common in Amaryllideae, while the rigid, radiating pedicels of some taxa allow the infructescences to bowl along in the wind. The testa is commonly massive, green and photosynthetic, and with anomocytic stomata in Amaryllidinae, while in Crinum, of the same tribe, it is the endosperm that is green and photosynthetic. Seeds of some species of Crinum lack a testa and have a corky outer endosperm; such seeds can float and remain viable in sea water for up to two years, while seeds of other species lack the corky layer, sink fast and can germinate without very much in the way of water at all (Snijman & Linder 1996; Bjorå et al. 2006). In Boophone and Cybistetes the seeds germinate while still in the fruit, and in Calostemmateae the bulbil, a precociously-germinated embryo, is the dispersal unit. The inflorescence of Gethyllis (Haemantheae, includes Apodolirion) has a single flower; the ovary is subterranean and the many-seeded fruit is indehiscent and may be sweetly scented when ripe; dispersal by small mammals?

Genes & Genomes. García et al. (2014) discuss the likelihood that there was extensive and ancient hybridization in Hippeastreae-Hippeastrinae, although not in -Traubiinae.

There has been a reduction in the GC content of the genome, perhaps associated with the large genome sizes also found here (Smarda et al. 2014).

Chemistry, Morphology, etc. Norbelladine alkaloids, unique to Amaryllidoideae, are tyrosine derivatives. There are over 200 different structures of which 79 or more are found in Narcissus alone (Martin 1987; Bastida & Viladomat 2002: other references in the same volume; Rønsted et al. 2008b). These alkaloids cause acetylcholinesterase inhibition, etc., in Haemantheae (Bay-Smidt et al. 2011) and Calostemmateae (Jensen et al. 2011). All told over 500 alkaloids placed in 118 different classes have been recorded from the subfamily (Rønsted et al. 2012); a number of species are poisonous because of them.

Because of the leaf fibres in Amaryllideae, the coverings of the bulbs produce highly-extensible cotton-like fibres when torn. There are often crystals of calcium oxalate in the epidermis.

The flowers of Galanthus are shown with the median member of the outer whorl in the adaxial position (Spichiger et al. 2004), see also the similar position in Hippeastrum and several other monosymmetric Amaryllidoideae. Some species of Phaedranassa have slit-monosymmetric flowers, with all the stamens, etc., leaving the flower via an abaxial slit in the perianth tube; I do not know details of the symmetry there. Flowers of some species of Crinum are monosymmetric. In Galanthus in particular the inner whorl of tepals is very different from the outer whorl, although both are petal-like.

The corona of e.g. Hymenocallis, evascularized outgrowths of the filaments, and that of Narcissus, vascularized and tubular (see also Scotland 2013), but not associated with the stamens, are quite different (e.g. Arber 1937); the corona may also be a tube, sometimes toothed (Pancratium), on which the stamens are born. Haemanthus has tepals with a single trace. In Strumaria and Carpolyza the bases of the filaments are adnate to the style, while in Strumaria and Tedingia the base of the style may be much inflated, even bulbous. Flowers of Gethyllis have up to 18 stamens.

Crinum has ategmic ovules and nuclear endosperm (Howell & Prakash 1990). In Hymenocallis caribaea the ovule is crassinucellate ("pseudocrassincellate"), the micropyle is zig-zag, and there is a massive, vascularized outer integument (Raymúndez et al. 2008). x = 11 may be the basal chromosome number for the family (Meerow et al. 2006). A very long-tubular dropper cotyledon sheath may develop during germination.

For general information, see Markötter (1936: some South African taxa) and Meerow and Snijman (1998), and for anatomy, see Arroyo and Cutler (1984), for pollen, see Dönmez and Isik (2008), and for embryology, see Stenar (1925).

Phylogeny. Phylogenetic relationships within Amaryllidoideae are [Amaryllideae [Cyrtantheae [Calostemmateae, Haemantheae, Gethyllideae [Eurasian Clade [Andean Clade, Extra-Andean Clade]]]]] (Meerow et al. 1999, 2000a, 2000b). Relationships between major clades of American and some southern African members are not well understood, furthermore, Meerow et al. (2006) found that the inclusion of Hannonia, Lapiedra and Vagaria destabilised relationships in the European clade; Lledó et al. (2004) included the last two in Galantheae. Meerow and Clayton (2004) discussed relationships among African taxa. In a more recent study using genes from all three compartments and sampling 108 species recovered the relationships [Amaryllideae [[Calostemmateae [Cyrtantheae + Haemantheae]] [Eurasian Clade [Andean Clade, Extra-Andean Clade]]]], although support for some nodes was poor (Rønsted et al. 2012: see classification above). Meerow et al. (2006) provide a phylogeny for the Eurasian Clade, which includes daffodills, snowdrops, etc. The main dichotomy separates the Central and East Asian Lycorideae from the rest, which centre on the Mediterranean region. ITS and ndhF phylogenies are not congruent (Meerow & Snijman 2006).

Meerow and Snijman (2001, see also 2006) discuss relationships within Amaryllideae; Amaryllis and Boophone are successively sister to the rest of the tribe. Amaryllis differs from other Amaryllidineae in not having a green testa, etc. Meerow et al. (2003) outline the phylogeny of Crinum, the only pantropical member of Amaryllidaceae; see also Kwembeya et al. (2007). For a phylogeny of Cyrtanthus (Cyrtantheae) and discussion on its evolution, see Snijman and Meerow (2010); molecules and cytology, but less so morphology, tend to agree, and the old species groupings, based on floral (pollinator) morphology, have broken down. For relationships in Haemantheae, see Conrad et al. (2006) and Bay-Smidt et al. (2011); Gethyllis was embedded in Haemantheae (Rønsted et al. 2012). For a phylogeny of Galantheae and its alkaloids, see Lledó et al. (2004) and Larsen et al. (2010), and for that of Narcissus, see Rønsted et al. (2008b: acetylcholinesterase-inhibiting alkaloids) and Santos-Gally (2012).

Relationships are reticulating in many Hippeastreae-Hippeastrinae (García et al. 2014). Worsleya and Griffinia are morphologically and phylogenetically isolated - n = 10, 21; velamen + [Worsleya]; flowers blue; seeds whitish, globose, turgid [Griffinia] (Meerow et al. 2000a).

Classification. For the infrafamilial classification of Amaryllidaceae, I follow Chase et al. (2009). For a classification of Amaryllideae, see Meerow and Snijman (2001), and for generic limits in Galantheae, see Lledó et al. (2004).

Botanical Trivia. The "Amaryllis" of many a windowsill is in fact a Hippeastrum.

ASPARAGACEAE Jussieu, nom. cons.   Back to Asparagales


153/2,500. World-wide, but not Arctic - seven groups below.

Age. Divergence within the crown group began ca 89 m.y.a. (Janssen & Bremer 2004). Eguiarte (1995: Agavaceae and Nolinaceae), however, suggested an age of only some ca 47 m.y.a., Bell et al. (2010) suggested a crown-group age of (66-)56, 51(-42) m.y., while estimates in S. Chen et al. (2013) are (65-)56(-48) or ca 36.4 m. years.

Evolution. Divergence & Distribution. Note that some of the ages given for nodes in this clade by S. Chen et al. (2013) suggest conflicting topologies.

There are no obvious apomorphies for Asparagaceae s.l., however, "endosperm helobial, thick-walled, pitted, hemicellulosic" might be placed at this level. The homoisoflavanones found in Scilloideae are rather uncommon in flowering plants, but they are also found in Camassia (Agavoideae, ex Chlorogaloideae) and Ophiopogon (Nolinoideae).

Phylogeny. These seven subfamilies form a rather well supported clade in Fay et al. (2000). Fay et al. (2000), Pires et al. (2001), and Pires and Sytsma (2002) discuss uncertainties as to the immediate sister taxon to Themidaceae (= Brodiaeoideae). Aphyllanthes has a very long branch in the three-gene analysis of Fay et al. (2000), and its phylogenetic position is unclear; its removal from analyses can rather dramatically changes support values (Chase et al. 2006). A position close to Hyacinthaceae (= Scilloideae) was found by McPherson and Graham (2001), but Pires et al. (2006) place it sister to Laxmanniaceae (= Lomandroideae), albeit with weak support. The [Themidaceae + Hyacinthaceae] clade is moderately well supported (Fay & Chase 1996; Meerow et al. 2000), but support in the two-gene analysis of Jang and Pfosser (2002: Aphyllanthes not included) is only weak (see also Chase et al. 2006; Pires et al. 2006). Seberg et al. (2012) found the relationships [[Brodiaeoideae + Scilloideae] [Aphyllanthoideae + Agavoideae]], but the position of Aphyllanthes had no support. Steele et al. (2012) also found Aphyllanthes associating with this group, but again with little support; there was good support for a clade [Lomandroideae [Asparagoideae + Nolinoideae]] (for this latter clade, see also Fay et al. 2000: moderate support; Seberg et al. 2012, strong support). A placement of Eriospermum (Nolinoideae here) as sister to Asparagoideae has quite strong support (Seberg et al. 2012); this position must be confirmed, while Eguchi and Tamura (2016) retrieved a clde [ Nolinoideae [Asparagus + Cordyline], although relationships at this level were not their focus. For details of relationships, see also Bogler et al. (2006).

Classification. This is a highly unsatisfactory family. Nothing characterises it, and while some of the subfamilies have several distinctive apomorphies and are also easy to recognise, others are difficult to recognise. The flowers of the whole group are for the most part a rather undistinguished "lily"-type, and quite often are rather small. Asparagoideae, and especially Nolinoideae and Agavoideae, are very heterogeneous, several families having been segregated from them in the past. For the use of Asparagaceae s.l. to refer to the entire clade, c.f. A.P.G. II (2003) and A.P.G. III (2009). The subfamilial classification follows that in Chase et al. (2009b), but I have also included familial names for each clade, in part because the roots of the two sets of names differ in over half the cases and both will be encountered in the literature.

[Aphyllanthoideae [Agavoideae [Brodiaeoideae + Scilloideae]]: ?

Age. The age of this node is (59-)50(-41) or ca 40.5 m.y. (S. Chen et al. 2013: c.f. dates for Agavoideae).

1. Aphyllanthoideae Lindley   Back to Asparagales


Flavonols +; vessel elements in roots often with simple perforation plates; secondary growth +; stems alone photosynthetic, with parallel wax scales; leaves two-ranked, vernation supervolute-subinvolute, scaly, non-photosynthetic, ligulate, base?; inflorescence scapose, flowers multibracteolate, sessile; T marcescent, basically free, with a single trace; A adnate to base of T; pollen spiraperturate; ovary sulcate down middle of loculus; infra-locular septal nectaries +, stigma trifid, dry; ovule 1/carpel, micropyle?; seeds slightly flattened, exotestal cells large, isodiametric; endosperm ?, 0; n = 16; cotyledon photosynthetic, terete, first leaf terete.

1[list]/1: Aphyllanthes monspeliensis. W. Mediterranean. [Photo - Flower © E. Bourneuf.]

Synonymy: Aphyllanthaceae Burnett

Chemistry, Morphology, etc. The stomata are in bands down the scape. The tepals have but a single bundle. Is there chelidonic acid?

General information is taken from Conran (1998); he mentions helobial endosperm development here, but c.f. Schnarf and Wunderlich (1939), apparently the only source of embryological information.

[Agavoideae [Brodiaeoideae + Scilloideae]]: ?

Age. The age of this node is estimated at (62-)51, 46(-37) m.y. by Bell et al. (2010) and at ca 49.8 or 33.5 m.y. by S. Chen et al. (2013).

2. Agavoideae Herbert   Back to Asparagales


Plant rhizomatous; endosperm helobial, thick-walled, pitted, hemicellulosic.

23/637 [list] - five groups below. More or less world-wide, esp. S.W. North America, few in Malesia, N. Australia, not cold temperate, New Zealand, etc. (map: see Ying et al. 1993; García-Mendoza & Galván V. 1995; Fl. N. Am. 26: 2002; Seberg 2007).

Age. Crown-group Agavoideae can be dated at (76-)61.5(-47.5) m.y. (McKain et al. 2016c) or (53-)42.5(-34) or ca 19.9 m.y.a. (S. Chen et al. 2013: perhaps).

2A. Anemarrheneae Reveal

Leaves ?spiral, base?; inflorescence subspicate, branched; T ± free; A 3, opposite and adnate to middle of inner T; ovules 2/carpel, apotropous; seeds angled; embryo curved; n = 11; hypocotyl 0.

1/1: Anemarrhena asphodeloides. N. China, Korea.

Synonymy: Anemarrhenaceae Conran, M. W. Chase & Rudall

[Agaveae [Behnieae [Herrerieae + Anthericeae]]]: (vessels in stem); nucellar cap, hypostase +.

Age. The age of this node is some (56-)41.5(-26.5) m.y. (McKain et al. 2016c), (48-)40, 33(-23) m.y. (Bell et al. 2010), 36-35 m.y. (Wikström et al. 2001) or 34.2-29.1 m.y. (Good-Avila et al. 2006).

This group has 100% support in three- and four-gene trees (Chase et al. 2000a; Fay et al. 2000; Bogler et al. 2006).

2B. Agaveae Dumortier / the ABK clade [Agavoideae bimodal karyotype clade]

Also caulescent, (bulbs, tunicated or not); non-protein amino acids, saponins, (homoisoflavanones - Chlorogalum), flavonols +; (monocot secondary thickening +); (silica bodies in bulb - Polianthes); adaxial bundles in leaf inverted [?level]; also styloids +; (stomata para- or tetracytic), cuticular wax rodlets parallel; (rhexigenetic lacunae + - Chlorogalum, etc.), leaves spiral, (petiolate), (often fleshy), (margins serrate), apex (pungent-)pointed, base ?; inflorescence usually branched, and/or flowers in pairs or fascicles, (pedicel articulated - Chlorogalum, etc.); flowers large, (monosymmetric); tapetal cells several-nucleate; pollen semitectate, (operculate); ovary superior to inferior, (styles +; with 3 canals - Camassia), stigma wet to dry; ovules many/carpel, outer integument (4-)9-14 cells across, (parietal tissue -2 cells across), (nucellar cap 2 cells across), ± postament, hypostase, obturator +; (capsule septicidal - some Yucca), (fruit a berry), T marcescent; seeds flattened [?all]; (endosperm thin-walled - Hosta), (perisperm +, oily - Yucca, Agave); n = 30, chromosomes bimodal [25 short + 5 long], (7, 12, 18 S + 5, 3, 6 L), 0.4-10 µm long; genome duplication; (cotyledon non-photosynthetic - Funkia), hypocotyl to 4 mm long, collar rhizoids +, primary root often branched.

10/340 (?600): Agave (220), Yucca (50), Hosta (23). Central U.S.A. to N. South America, mostly S.W. North America, also East Asia (Hosta). [Photo - Flower.]

Age. Crown-group Agaveae are (37.5-)28(-20.5) (McKain et al. 2016c), (33.4-)25.8, 20.5(-18.4) (Good-Avila et al. 2006) or (33.4-)23.7(-14) m.y.o. (Smith et al. 2008).

Synonymy: Agavaceae Dumortier, nom. cons., Chlorogalaceae Doweld & Reveal, Funkiaceae Horaninov, nom. illeg., Hesperocallidaceae Traub, Hostaceae B. Mathew, Yuccaceae J. Agardh

[Behnieae [Herrerieae + Anthericeae]]: ?

Age. The age of this node is some (34-)24, 22(-13) m.y. (Bell et al. (2010).

2C. Behnieae Reveal

± Sprawling, rhizomatous; monocot secondary thickening +; tannin cells 0; velamen 1-layered; vessel elements also in the stem; leaves two-ranked, "supervolute", petiolate, blade broad, with midrib and transverse tertiaries, leaf base not sheathing; dioecious; A adnate to base of T; ovules 2-3/carpel, micropyle?, parietal tissue none; stigma 3-lobed, wet; fruit a berry, T marcescent, not twisting; seeds angular, phytomelan 0, testa and tegmen thin-walled; endosperm walls not pitted and hemicellulosic; n = ?

1/1: Behnia reticulata. Zimbabwe to eastern South Africa.

Synonymy: Behniaceae Conran, M. W. Chase & Rudall

[Herrerieae + Anthericeae]: (monocot secondary thickening +).

2D. Herrerieae Baillon

Usu. climbers, prickly; saponins +, chelidonic acid?; (vessel elements in stem); mucilage cells 0; cuticular wax rodlets parallel; leaves spiral, fasciculate, sheath?; pedicels not articulated; T and A free; ovules 1-many/carpel, parietal tissue?; fruit a septicidal capsule; seeds flattened; "embryo short"; n = 27, dimorphic [one large], chromosomes 0.7-3.7 µm long [Herreria]; "germination epigeal".

2[list]/9. South America (Brazil southwards), Madagascar. [Photo - Fruit.]

Synonymy: Herreriaceae Kunth

2E. Anthericeae Bartling

Rhizome short; chelidonic acid +; (velamen +); (vessel elements in the stems); mucilage cells +, tannin cells 0, (styloids + - Chlorophytum); cuticular wax rodlets parallel; leaves spiral to two-ranked, base sheathing; inflorescence thyrsoid (raceme); (pedicels not articulated); (flower monosymmetric), (T tube 0); (pollen mixed with raphides); stigma dry; ovules 2-many/carpel, outer integument ca 4 cells across; embryo sac haustoria common; T persistent in fruit; seeds angular or flattened, tegmen?; embryo curved or angled; n = 7, 8, 10, 11, 13-15, etc., chromosomes 2-10(-13.8) µm long, genome duplication [Chlorophytum]; cotyledon not photosynthetic, coleoptile + [Chlorophytum].

8/285: Chlorophytum (150), Anthericum (65), Echeandia (60). More or less worldwide, but not cold temperate, few in Malesia, N. Australia, not New Zealand, etc. [Photo - Inflorescence, Flower.]

Synonymy: Anthericaceae J. Agardh

Evolution. Divergence & Distribution. Good-Avila et al. (2006) suggest that Agave et al. are only some 26-20 m.y.o., and Yucca 18-13 m.y. old. Rocha et al. (2006) suggest ca 12.75 m.y. as the age of Agave etc. and ca 10.2 m.y. for Agave s.l. (Hesperaloe and everything above in the tree - Bogler et al. 2006; c.f. also Smith et al. 2008); there are yet other possibilities for dates.

Good-Avila et al. (2006) discussed diversification in both Agave, which they thought was connected with the adoption of bat-pollination, and Yucca (see also Rocha et al. 2006). Smith et al. (2008) suggested that diversification was not significantly different in Yucca, with 34(-50) species, and Agave, with some 250 or more species. They found little evidence that the adoption by Yucca of its remarkable pollination mechanism increased its diversification rate, even although its sister group is considerably smaller. Pulses of diversification in agaves may have happened a mere 9-6 m.y.a., a time when other succulent clades were diversifying (e.g. Good-Avila et al. 2006; Arakaki et al. 2011).

Ecology & Physiology. Nobel (1988) discussed the eco-physiology of agaves and their relatives. Over 300 species are succulents, mostly leaf succulents (Nyffeler & Eggli 2010b); drought tolerance is common, and some species in the Chlorogalum area grow on serpentine soils, themselves often subject to drought (Halpin & Fishbein 2014).

The CAM photosynthetic pathway has evolved ca three times in Agaveae, a major CAM clade, and is found in nearly all species of Agave (there seems to have been a reversal in Polianthes [= Yucca] tuberosa, at least), Yucca subgenus Sarcocarpa and Hesperaloe (Heyduk et al. 2016). Interestingly, succulent leaves with a three-dimensional venation system that are characteristic of the CAM species are also found in related C3 species, and the CAM-type morphology may have evolved before CAM photosynthesis itself (Heyduk et al. 2016).

Pollination Biology & Seed Dispersal. The Yucca-yucca moth (Tegeticula, Parategeticula: Prodoxidae) association has been a textbook example of mutualism or co-evolution, the two partners showing reciprocal evolutionary change (see Althoff et al. 2012 for details); a similar pollination association in Hesperoyucca seems to have evolved independently (McKain et al. 2016). The association may be some 40 m.y.o. (c.f. some dates above), Pellmyr & Leebens-Mack 1999) estimating that the beginning of the association was around (51.5-)41.5(-31.5) m.y.a., active pollination by Tegeticula and Parategeticula beginning (44.5-)35.5(-26.5) m.y.a. (see also Pellmyr et al. 1996, 2007; ; Pellmyr 2003; Gaunt & Miles 2002; Althoff et al. 2006; Smith et al. 2008), but there may have been another and more recent radiation of yucca moths only 3-2 m.y. ago. On the other hand, crown Yucca was aged at (14.5-)12.5(-11.5) m.y., the stem age being ca 20 m.y., the stem age of Hesperoyucca being (24-)16.5(-9) m.y. (McKain et al. 2016c). Tegeticula pollinates Hesperoyucca, the species of the former that is the pollinator being sister to the rest of the genus, suggesting that this association is pretty old (Pellmyr & Leebens-Mack 1999; McKain et al. 2016c)Close relatives of yucca moths also eat Dasylirion and Nolina (see Nolinoideae) and other Prodoxidae are found on Saxifragaceae (Saxifragales); the ancestral condition for yucca moths may have been to eat ovaries (Yoder et al. 2010). Prodoxus, not a pollinator but a specialist herbivore on Yucca, and Parategeticula, another pollinator, are also involved; all told, there are over 22 species of pollinating moths, 2-3 species of cheater moths, and over 35 species of Yucca (Althoff 2016 and references). Much of the divergence in Yucca seems to have occurred before that of its main pollinator but only a mere 6-4 m.y.a., and given the vagility of the moth, it is difficult to imagine how strict co-evolution might work (see also Godsoe et al. 2010; Starr et al. 2014; Hembry et al. 2014). Initial diversification in Yucca may have been in association with Parategeticula, a poor flier and now rather uncommon (Althoff et al. 2012).

For the pollination biology of Agaveae, see Rocha et al. (2006), and for diversification in Yucca compared with that in its relatives, see above.

Bat pollination is common in the large genus Agave and its relatives (Fleming et al. 2009).

Plant-Animal Interactions. Caterpillars of the giant skippers, found in Mexico and the adjacent southwest U.S.A., bore tunnels in the roots and leaves of Agave and Yucca (Warren et al. 2009).

Genes & Genomes. For a connection between the evolution of the bimodal karyotype of Agave, Hesperocallis, and their relatives and polyploidy, see McKain et al. (2011, 2016a, esp. 2012) and Halpin and Fishbein (2014). Hesperocallis has 4 long, 2 medium and 18 short chromosomes, and there are other combinations (Halpin & Fishbein 2014; McKain et al. 2016c), but details of how bimodality interacts with polyploidy are unclear. The switch from the 25 short + 5 long in North American Agaveae tends to be linked with the adoption of more mesic habitats and corresponding morphological changes (McKain et al. 2016c).

At least some mitochondrial genes show an accelerated rate of change (G. Petersen et al. 2006).

Chemistry, Morphology, etc. Agave is rich in saponins and sapogenins (Sidana et al. 2016).The raphides of Agave are hexagonal in transverse section. For variegation in Hosta, see Zonneveld (2007). The leaves of Herreria and Herreriopsis are described as being cladode-like (Conran 1998) or cladodes (Stevenson in Takhtajan 1997).

The flowers of Agave are shown with the median member of the outer whorl in the adaxial position (Spichiger et al. 2004). Camassia at least has single-trace tepals, Agave, etc. have three, while Hosta may have as many as 13 (Lin et al. 2011). The outer tepals of Herreriopsis have sac-like bases - possibly tepalline nectaries. In Hosta the stamens are sometimes inserted on the ovary. The tapetal cells of Polianthes (= Agave) are multinucleate. Germination of the pollen grain via the proximal pole has been reported in Beschorneria (Hesse et al. 2009a). Furcraea has nuclear endosperm.

Traub (1982) noted that Hesperocallis undulata smells of onions, and he even associated it with his Alliales. The genus was geographically odd in Hostaceae s. str., which is where other workers had placed it (c.f. Kubitzki 1998b), but not in Agavoideae as here circumscribed; now Hosta is a little odd from the geographical point of view.

The ovary and fruit of Leucocrinum (Anthericum group) are below the surface of the ground (Bogler et al. 2006). Some information is taken from Conran (1998); ovule morphology is known from Leucocrinum alone in this group.

Ubisch bodies are present in Anemarrhena, so there is probably a glandular tapetum. Information is taken from Conran and Rudall (1998 - confusion over stamen position) and Rudall et al. (1998b). For information about Behnia, Herreria and Herreriopsis, see Conran (1998); details of ovules/embryology are unknown.

See Verhoek (1998) and Judd et al. (2007) for general information; for additional information, especially on the part that has been considered Agavaceae s. str. in the past, i.e. Agave, Yucca and their immediate relatives, see Lynch et al. (2001: c.f. Scilloideae!) and Solano et al. (2013: Polianthes anatomy), Alvarez & Köhler (1987: pollen), Fagerlind (1941b), Cave (1948, 1955), Wunderlich (1950: also floral morphology) and di Fulvio and Cave (1965), all embryology; see also Kubitzki (1998b - Hostaceae), Speta (1998 - Hyacinthaceae-Chlorogaloideae).

Phylogeny. For relationships within this clade, see Pires et al. (2004) and especially Bogler et al. (2006: 2- and 3-gene analyses, the latter with missing data, but overall the same topology). I have followed the latter - which see for more details - in the topology above. Support for the subfamily as a whole is only 75%, that for the [Behnia + Herreria, etc. + Anthericum, etc.] clade 87%, and that for [Herreria, etc. + Anthericum, etc.] only 51% (and still less in the two-gene tree); however, other nodes have close to 100% support. Largely similar relationships were found by G. Petersen et al. (2006c) in their analysis of variation of four mitochondrial genes that are evolving particularly quickly in this clade. Smith et al. (2008) included Hosta, etc., in their Agavaceae and excluded Anthericaceae, although support for Agavaceae so delimited was weak; that for the still broader circumscription adopted here was stronger.

The circumscription of group 4b above, Agave, etc. + Hesperocallis, or the ABK clade, corresponds to that of Agavaceae s.l. in Bogler et al. (2006). There is a fair amount of resolution of relationships around Agave and Yucca. Agave includes Manfreda, Polianthes, etc., and [Beschorneria + Furcraea] are sister to Agave s.l.. The position of Yucca is unclear, but it may well be sister to that combined clade (Bogler et al. 2006; Archibald et al. 2015; McKain et al. 2016c). Hesperocallis undulata was sister to that clade (Bogler et al. 2006), although it has also been placed sister to a clade that includes many ex-Chlorogaloideae (Halpin & Fishbein 2013; see also Archibald et al. 2014, esp. 2015), i.e. [Hesperocallis [paraphyletic Chlorogalum [Camassia + Hastingsia]]], there is a well-supported [Hesperoyucca [Hesperoaloe + Schoenolirion]] clade, although exactly where it might go is unclear (see also McKain et al. 2016: sister to the immediately preceding clade), and ,i>Hosta

is sister to the rest of this whole clade. Within Camassia there is a fair bit of resolution (Fishbein et al. 2010; Halpin & Fishbein 2013; Archibald et al. 2015). For other phylogenetic work on this group, see also Eguiarte et al. (1994), Bogler and Simpson (1996: molecular) and Sandoval (1995: morphological).

Classification. The broad concept of Agavoideae adopted here may not seem very satisfactory, but none of the alternative solutions is any better. Agave should probably include Polianthes, Manfreda, etc., see e.g. Bogler and Simpson (1995), Bogler et al. (2006) and Rocha et al. (2006).

Previous Relationships. Paradisea (ex Asphodelaceae/Xanthorrhoeaceae-Asphodeloideae) is a member of the Anthericum group (e.g. Chase et al. 2000b). Behnia was included in Luzuriagaceae (Liliales here) by Taktajan (1997), but it has also been placed in other lilialean and asparagalean families (Bogler et al. 2006); Camassia, etc., used to be in Liliaceae (Cronquist 1981) or Hyacinthaceae-Chlorogaloideae. Patil (2015) included four unrelated groups in his Agavaceae.

[Brodiaeoideae + Scilloideae]: steroidal saponins +; leaves spiral; inflorescence scapose, pedicels bracteate; raphides in carpel wall; ovules anatropous; endosperm helobial or nuclear; cotyledon not photosynthetic.

Age. The age of this node is estimated at (56-)45, 40(-15) m.y. by Bell et al. (2010) and at (58-)48(-40) or around 40.6 m.y. by S. Chen et al. (2013).

Evolution. Divergence & Distribution. For some other characters of this pair, see Fay and Chase (1996); laticifer-like structures may occur in both.

3. Brodiaeoideae Traub   Back to Asparagales


Plant monopodial, cormose, storing starch; sheath fibrous; laticifers +; mucilage cells?; leaves (unifacial - Brodiaea), sheath closed; inflorescence umbellate, cymose, inflorescence bracts several, scarious, also internal bracts; pedicels often articulated; (T free; corona +); A (3), connate and/or adnate to T, (filaments flattened); (ovary stipitate, adnate to T by flanges opposite the outer tepals), stigma capitate to trifid, dry (wet - Bloomeria); ovule with outer integument 3-4 cells across, (inner integument 3+ layers across), parietal tissue 3-4 cells across, (nucellar cap +); seeds angular, cells of tegmen much enlarged (not - Triteleia); (endosperm helobial - Muilla, Triteleia), "embryo short"; n = 5-12+; hypocotyl?, primary root persistent.

12[list]/62. S.W. North America, to British Columbia and Guatemala (map: see Moore 1953; Fl. N. Am. 26: 2002). [Photo - Flower, Flower, Fruit.]

Age. Divergence within Brodiaeoideae began around 25.1 or (26-)20(-24) m.y.a. (S. Chen et al. 2013).

Synonymy: Themidaceae Salisbury

Chemistry, Morphology, etc. Little is known about the chemistry of Brodiaeoideae.

When the tepalline tube is adnate to the stipitate gynoecium, three narrow, ?nectar-containing tubes are formed. Embryologically Brodiaeoideae are quite variable. The inner integument is massive or not, ditto base of the nucellus, endosperm development varies, etc. (Berg 1978, 2003 for a summary).

Some information is taken from Rahn (1998: general) and Moore 1953 (morphology).

Phylogeny. There are two major clades, [Muilla, Triteleia] and [Dipterostemon, Dichelostemma, Brodiaea], albeit with only moderate support. The first clade has a long tepalline tube and the second has appendages on the bases of the filaments that form a nectar cup; both characters arise in parallel in the two clades (Pires & Sytsma 2002; c.f. Seberg et al. 2012). See also Pires et al. (2001) for phylogeny and morphological evolution.

Previous Relationships. Themidaceae/Brodiaeoideae have often been included in Alliaceae/Amaryllidaceae-Allioideae because of their superficially similar umbellate inflorescence and rather undistinguished monocot flowers (e.g. Takhtajan 1997).

4. Scilloideae Burnett  Back to Asparagales


Plant bulbous, geophytic, roots often contractile; endomycorrhizae 0; polyhydroxyalkaloids, homoisoflavones, flavone C-glycosides +; little sclerenchyma in the leaf (well-developed); mucilage cells +; (leaf waxes with parallel platelets); bulb leaf sheaths closed or not; inflorescence scapose [?all], (branched), (spike), pedicels not articulated, bracteole 0; (corona +); stigma capitate to punctate and papillate; ovules 1-many/carpel, outer integument 2-4 cells across, parietal tissue 1-4 cells across, (nucellar epidermis radially elongated), nucellar cap +/0, raphides +, obturator +; (suprachalazal area long, with central column of cells - Drimiopsis [= Ledebouria); seeds black; testa multi-layered; chromosomes 1.2-18 µm long; nucleus with protein crystals; (hypocotyl 0; collar rhizoids +).

41-70[list]/800-1025 - six groupings below. Predominantly Old World in Mediterranean climates, esp. S. Africa and the Mediterranean, to Central Asia and Japan; a few in South America (map: both colours).

Age. Oziroë diverged from the rest of the clade in the Oligocene ca 28 m.y.a. (Ali et al. 2012).

4A. Oziroëeae M. W. Chase, Reveal & M. F. Fay

A basally connate and adnate to C; seeds rounded, surface rugose; embryo long; n = 15, 17; cotyledon?

1/5. Western South America (map: see above, green, from Guaglianone & Arroyo-Leuenberger 2002).

[Ornithogaleae + Urgineeae + Hyacintheae]: fructan sugars accumulated; rhexigenetic lacunae +; also styloids +; (pollen mixed with raphides).

Age. The beginning of divergence within this clade can be dated to (47-)37(-29) or around 25.2 m.y.a. (S. Chen et al. 2013).


4B. Ornithogaleae Rouy

Cardenolides +; roots not medullated; (A 3; filaments flat, with appendages); seeds flattened/angled; protein crystals in nucleus; n = 2-10+; cotyledon photosynthetic or not.

4/312: Ornithogalum (160), Albuca (110-140). Europe, W. Asia, Africa.

Synonymy: Ornithogalaceae Salisbury


4C. Urgineeae Rouy

Bufadienolides +; bracts spurred-peltate [as small leaves in Bowiea]; (stylar canals 3 - Boweia); seeds flattened/winged; testa brittle, not tightly adherent to endosperm; n = 6, 7, 10+ [x = 10]; nucleus without protein crystals.

2(-3?)/105: Drimia (100). Mainly Africa, Madagascar, the Mediterranean to India (map: from Pfosser & Speta 2001). [Photos - Boweia Collection.]

4D. Hyacintheae Dumortier

Homoisoflavanones +; (leaves with pustules or coloured spots); T with a single trace; embryo sac variable, e.g. bisporic [micropylar dyad], 8 nucleate [Endymion-type]; seeds (brown to yellow), usu. rounded; elaiosomes common; x = 10.

Age. Crown Hyacintheae are ca 18.8 m.y.o. (Ali et al. 2012).

Massoniineae, Pseudoprosperoineae

a. Pseudoprosperineae J. C. Manning & Goldblatt

(Inflorescence branched); bracteole +, ± lateral; 2 ovules/carpel; 1 seed/loculus; n = 9; cotyledon not photosynthetic.

1/1: Pseudoprospero firmifolium. Southeast South Africa (Map: blue-green).

[Massoniinae + Hyacinthinae]: ?

Age. The age for this node is ca 17.9 m.y. (Ali et al. 2012).

b. Massoniinae Bentham & Hooker f.

(Bracteole +); (flowers monosymmetric); ovary and style sulcate, style with 3 canals; ovules 2-many/carpel; (elaiosomes +); n = 5-10+, many 20 [x = 10]; cotyledon not photosynthetic (photosynthetic).

Ca 10/260: Lachenalia (135), Ledebouria (70). Africa S. of the Sahara, Ledebouria to India (map: above, from Venter 2008, red, including blue-green area).

Age. Crown Massoniinae are ca 16.3 m.y.o. (Ali et al. 2012).

Synonymy: Eucomidaceae Salisbury, Lachenaliaceae Salisbury


c. Hyacinthinae Parlatore

Endomycorrhizae +; (bracts 0), prophylls quite common; stylar canal papillate; ovules 2-8(-many)/carpel, outer integument 4-5 cells across, parietal tissue 2-3 cells across; antipodal cells large; (elaiosomes +); n = 4-8+ [x = 9]; cotyledon photosynthetic or not.

21/265: Muscari (50), Bellevalia (50), Scilla (30), Prospero (25). Europe (not the northeast), the Mediterranean, the Mid East, North Africa, Barnardia japonica in the Far East (map: Meusel et al. 1965). [Photo: Scilla Collection.]

Age. Crown Hyacinthinae are ca 15.3 m.y.o. (Ali et al. 2012).

Synonymy: Hyacinthaceae Borkhausen, Scillaceae Vest

Evolution. Divergence & Distribution. Hyacintheae may have originated in sub-Saharan Africa and dispersed north and also east, but details depend on the analytic method used (Ali et al. 2012). There are about 300 species of Scilloideae in the Cape flora alone (Procheŝ et al. 2006), about 400 species in southern Africa (Johnson 2010).

Ecology & Physiology. Many species in the foggy deserts of Namaqualand, South Africa, have water-catching leaves with very distinctive morphologies (Vogel & Müller-Doblies 2011).

Pollination Biology & Seed Dispersal. Lachenalia has monosymmetric flowers in which the median member of the outer whorl is in the adaxial position. The same is true of the remarkable monosymmetric flowers of Massonia (Daubneya) aurea that are on the outside of the inflorescence. These flowers have the three abaxial tepals greatly enlarged, while the inner flowers are polysymmetric, the tepals forming a simple, lobed tube; the result is an inflorescence looking like a flower. Pollination in Albuca is noteworthy in that the pollen is deposited by leaf-cutter bees on the tips of the inner tepals, but pollination is not completed until two to three days later when the flower withers, the tepals then press against the stigma, and the pollen finally germinates (Johnson et al. 2009b, 2012).

Species with myrmecochorous seeds are scattered throughout the subfamily (Lengyel et al. 2010).

Vegetative Variation. Some species of Scilloideae have terete, unifacial leaves, as in Ornithogalum, where they develop from the upper part of the leaf (Kaplan 1973). Even the bulb scales of some species of Rhadamanthus (= Drimia) are terete. Urgineeae have a backwardly-directed process at the base of the leaves and/or bracts (c.f. Asparagus-Asparagoideae). Vegetative variation - in both leaf and bulb - is also considerable in Ledebouria (Venter 2007). However, there is less anatomical variation.

Genes & Genomes. High C values in Scilla are associated with long cell cycles, as has been noticed elsewhere (Francis et al. 2008).

Chemistry, Morphology, etc. Bufadienolides are cardiac glycosides. Although mucilage cells are particlarly common in Scilloideae, they also occur elsewhere (Lynch et al. 2006).

For some floral vasculature, see Deroin (2014). Some Scilloideae have a filament tube. Wunderlich (1937) described the endosperm as being both helobial and nuclear in Hyacinthineae. Karyotypes may be bi- or even trimodal. The leaves of seedlings are two-ranked.

Information is taken from Speta (1998a: subfamilial classification of Hyacinthaceae, 1998b: general, 2001: subfamilial characters) and Pfosser and Speta (1999); for chemistry, see Kite et al. (2000), Pfosser and Speta (2001) and Koorbanally et al. (2008), for anatomy, see Lynch et al. (2001: leaf) and Sobotik and Speta (1997: root), for some embryology, see Sundar Rao (1940), Eunus (1950) and Berg (1962), for floral morphology in Ledebouriinae, see Lebatha and Buys (2006), and for cytology of some sub-Saharan members, see Goldblatt and Manning (2011) and Goldblatt et al. (2012: base numbers for tribes, etc.).

Phylogeny. The topology [Oziroëeae [Ornithogaleae [Urgineeae + Hyacintheae]]] has moderate support in Manning et al. (2004); Oziroë and Albuca (Ornithogaleae) were successively sisters to the rest at the base of Scilloideae in Seberg et al (2012), the position of the latter genus having only moderate support. There is little well-supported structure along the backbone of Hyacintheae and again within Hyacinthineae in the trnL-F spacer analysis of Wetschnig et al. (2002); the positions of Ornithogaleae and Urgineeae were also unclear. See also Pfosser et al. (2003, 2012), the latter dealing with relationships of the Malagasy taxa.

Classification. For a classification, see Speta (1998a: as Hyacinthaceae). There is considerable disagreement over generic limits here; are there 15 or 45 genera in sub-Saharan Africa? (e.g. Stedje 2001a, b; Pfosser & Speta 2001; Lebatha et al. 2006). See Speta (1998a) for the dismemberment of Scilla and Martínez-Azorín et al. (2011) for that of Ornithogaleae - 19 genera, of which 11 replace Ornithogalum; recognizability of taxa is not the issue. Manning et al. (2004) provide a generic synopsis of the family in sub-Saharan Africa that integrates some morphology with relationships; like them, I take a generally broad view of genera. However, there are unresolved issues that include sampling, whether or not floral syndromes distort ideas of relationships (and so what effect characters taken from these syndromes have in combined analyses), the consequences of maintaining well-known generic names like Albuca and Galtonia as knowlege of phylogeny becomes clearer, and the role cytological data should play. Albuca is recognized in the recent reclassification of Ornithogaloideae by Manning et al. (2009).

Previous Relationships. Chlorogaloideae, until recently included in Hyacinthaceae/Scilloideae (e.g. Pfosser & Speta 1999), are here included in Agavoideae.

[Lomandroideae [Asparagoideae + Nolinoideae]]: steroidal saponins +; pedicels articulated; fruit a capsule; endosperm helobial, thick-walled, pitted, hemicellulosic.

Age. For the age of this node, estimated at (59-)49, 45(-35) m.y., see Bell et al. (2010); (60-)50(-42) or around 32.7 m.y. are the estimates in S. Chen et al. (2013).

5. Lomandroideae Thorne & Reveal   Back to Asparagales

(Naphthoquinones +); (monocot secondary thickening +); (vessel elements in leaves); (T connate basally), ± dimorphic; infra-locular septal nectaries +; nucellar epidermal cells enlarged, supra-chalazal zone long, with central elongated cells; antipodal cells large; T persistent in fruit; seeds rounded to angular; cotyledon photosynthetic or not, (coleoptile +; first leaves reduced).

14-15[list]/178. Madagascar, India, South East Asia to the Pacific, and South America, predominantly Australian (Map: Fl. Australia vol. 46. 1986; Schlittler 1951).

Age. The crown group age of this clade is (57-)47(-39) or around 32.7 m.y. (S. Chen et al. 2013).


5Aa. Lomandra group

Plant ± rhizomatous; root tubers 0; leaf blade with sclerenchymatous ribs extending from the inner sheath of the vascular bundle to the surface, outer bundle sheath with enlarged cells; leaves two-ranked, flat or curved, (margins prickly), (base auriculate); pedicel articulated (not - Xerolirion); inflorescence units cymose [?all]; flowers long-lived; (pollen grains with encircling sulcus); stigma wet; ovules 1-2/carpel, nucellar cap +, nucellus with central conducting passage; testa lacking phytomelan, thin, tegmen brown, collapsed, cellular; endosperm hemicellulosic; n = 7-10, chromosomes 2-7 µm long.

5/65: Lomandra (50). Australia, New Guinea, New Caledonia (Map: Fl. Australia vol. 46. 1986; Australia's Virtual Herbarium xi.2014). [Photo - Inflorescence © K. Stüber.]

Synonymy: Lomandraceae Lotsy

5Ab. Sowerbaea group

Plant caespitose or rhizomatous, (stilt-rooted); (roots tuberous); leaves terete to triquetrous; inflorescence scapose (sessile), capitate to umbellate; (A 3, opposite inner T, staminodes 3 or 0 - Sowerbaea), (inner A adnate to T); stigma dilated or punctate; ovules 1-8/carpel; seeds dull brown to black, no aril, etc; n = 4.

2/18: Laxmannia (13). Southern Australia.

Synonymy: Laxmanniaceae Bubani


5B. Arthropodium group

Plant (rhizomatous), (climbing); roots often tuberous; (ecto)/vesicular-arbuscular mycorrhizae; mucilage +; leaves spiral, vernation supervolute or conduplicate, (petiolate), (ligulate); flowers single or in groups, long-lived, pedicel articulated or not; (inner T with long fimbriate/hairy margins); (A 3), (anthers dehiscing by pores), filaments with dense tufts of hairs [if inner T are not barbate]; stigma wet; nucellus with axial conducting tissue; seeds often arillate (strophiolate); testa with phytomelan, exotesta often papillate, rest of testa cellular, tegmen thin; endosperm thin-walled; n = 9-11, chromosomes 0.5-2 µm long.

6/74: Thysanotus (50), Arthropodium (20). South East Asia to Australia, New Zealand and the Pacific, Madagascar, C. Chile, Neuquén Province, Argentina (Map: Fl. Australia vol. 45. 1987; vol. 46. 1986; Schlittler 1951; Fl. China vol. 24. 2000; Australia's Virtual Herbarium xi.2014).

Synonymy: Eustrephaceae Chupov

5C. Cordyline group

Rosette herbs to trees; storage roots +; fructan sugars accumulated; mucilage +; stomata paracytic, subsidiary cells with oblique divisions; leaves spiral, vernation supervolute or conduplicate, (pseudopetiolate); flowers single, pedicel not articulated; testa with phytomelan, anatomy?; fruit a berry; endosperm ?; n = 3, 6, 19 (stamens dimorphic), chromosomes 0.5-2.4 µm long.

2/17. Mascarenes, India to the Pacific and New Zealand, tropical America (map: Fl. Australia vol. 45. 1987, vol. 46. 1986. [Photo - Habit, Flower.]

Chemistry, Morphology, etc. There are reports of cell wall ferulates from Xerolirion (Rudall & Caddick 1994), which, if true, makes it about the only non-commelinid genus with them. In Thysanotus roots, fungi are associated with the subepidermal layer of cells (McGee 1988).

Eustrephus has vessels in its leaves. The leaf of Lomandra and its relatives has sclerenchymatous ribs extending from the inner sheath of the vascular bundles (c.f. also Cordyline?). Lomandra was previously associated with Dasypogonaceae (Arecales), in which this sheath is absent, and Xanthorrhoea (Asphodelaceae, see above), where it comes from the mesophyll, although the leaves of all three are xeromorphic and superficially similar (Rudall & Chase 1996).

Xerolirion has solitary, terminal carpellate flowers, while its staminate flowers are in cymes. The pollen of Lomandra is very variable, sometimes being spiraperturate (c.f. Aphyllanthes). There is considerable variation in seedling morphology, even within individual groups (Conran 1998).

Additional information is taken from Schlittler (1951: Eustrephus), Chanda and Ghosh (1976: pollen, as Xanthorrhoeaceae), Chase et al. (1996), Conran (1998, as Lomandraceae), and Rudall (1994b, 2000: ovule, etc.).

Phylogeny. McLay and Bayly (2016) found two well supported clades in Lomandroideae. One included the [Chamaexeros + Lomandra] clade, with [Sowerbaea + Laxmannia] as its sister, the other was the [Trichopetalum + Murchisonia] clade; Cordyline may be sister to the latter. Relationahips found by S-C. Chen et al. (2013) are also in agreement, and for the Cordyline group, see Chase et al. (1996). Chamaescilla has been moved from Lomandroideae to Asphodelaceae-Hemerocallidoideae (McLay & Bayly 2016; see also).

Classification. I have tentatively recognised three groups above, partly based on morphology, and partly based on molecular data.

[Asparagoideae + Nolinoideae]: fructan sugars accumulated; (velamen +); flowers rather small[!]; T with a single trace; (fruit a berry); x = 10.

Age. The age of this node is estimated at (55-)44, 42(-34) m.y. by Bell et al. (2010) and at (57-)47(-37) or about 27.8 m.y. by S. Chen et al. (2013).

Chemistry, Morphology, etc. For ovule development, see Rudall (1994b).

Baccate fruits containing seeds that lack phytomelan are common here, but I do not know where they might be apomorphic. Since the capsular Hemiphylacus and [Comosperma + Eriospermum] are respectively sister to other Asparagaceae and Ruscaceae, baccate fruits are probably derived several times (c.f. Judd et al. 2007).

6. Asparagoideae Burmeister   Back to Asparagales


Herbaceous to shrubby, often climbers, or leaves in a rosette [Hemiphylacus], rhizome +, horizontal or vertical, root tubers +/0; flavonols, saponins +; (velamen +); vessel elements in roots often with simple perforation plates, vessels also in stem; cuticular wax rodlets parallel; leaves spiral, (scarious, often spiny - Asparagus), leaf base not sheathing, (cladodes +, flattened or terete - Asparagus); (plant mon- or dioecious); inflorescence ± fasciculate or paniculate; T tube at most short; A basally adnate to T, (3, opposite inner T, outer A staminodial); (G opposite inner T - Hemiphylacus), stigma wet or dry; ovules 2-several/carpel, outer integument ca 6 cells across, nucellar epidermal cells enlarged; embryo sac curved; (fruit a capsule - Hemiphylacus); seed rounded to ± angled; testa multiplicative, collapsing, exotesta massive, tegmen inconspicuous; endosperm cells thick-walled, pitted, embryo long; n = also 56 [Hemiphylacus], chromosomes 1-3 µm long.

2[list]/165-295: Asparagus (160-290!). Old World, but hardly in the Antipodes, also Mexico (map: from Hernandez S. 1995; Hultén & Fries 1986; FloraBase 2007; Seberg 2007; Kubota et al. 2011; B. Ford pers. comm. 2011; Trop. Afr. Fl. Pl. Ecol. Distr. 7. 2012: ?Malesia). [Photo - Flower, Fruit.]

Age. The start of divergence within crown group Asparagoideae can be dated to (25-)16(-9) or some 9.6 m.y.a. (S. Chen et al. 2013).

Synonymy: Hemiphylacaceae Doweld

Evolution. Divergence & Distribution. Fukuda et al. (2005a) and Norup et al. (2015) discuss diversification in Asparagus; this seems to have been rapid and to have started in southern Africa with several subsequent independent dispersal events to the north. Asparagus is quite often found in drier/sandy habitats.

Pollination. Hybridization between species seems common in the dioecious subgenus Asparagus (Kubota et al. 2011); dioecy seems to have evolved once in the genus (Norup et al. 2015). Species of Asparagus with flattened cladodes have perfect flowers (Kubota et al. 2011).

Vegetative Variation. There has been much discussion as to what the more or less leaf-like structures in the axils of the leaves in Asparagus "are" - stem or leaf or something else? (see e.g. Arber 1924b - prophyllar, axial; Cooney-Sovetts & Sattler 1986 - homeotic). Nakayama et al. (2012, see also Nakayama et al. 2010) looked at the development of both leaf-like and terete cladodes in Asparagus. The former (A. asparagoides) had an inverted (= prophyllar) orientation, while the latter (A. officinalis) were ventralised (c.f. Allium). They noted that both "leaf" and "stem" genes were expressed in the cladodes; the gene regulatory network for leaf development had been coopted by the axillary shoot (Nakayama et al. 2013).

Chemistry, Morphology, etc. Methyl mercaptans are known from Asparagus. Mucilage polysaccharides in the roots may have a storage role.

The prophylls ("bracts") at the bases of the pedicels in Hemiphylacus are described as being lateral (Hernandez S. 1995). For floral development in Asparagus, see Park et al. 2(003, 2004); b-class genes are not expressed in the outer tepal whorl.

Some information is taken from Robbins and Borthwick (1925: ovule and seed), Kubitzki and Rudall (1998: general) and Rudall et al. (1998b).

Phylogeny. For phylogenetic relationships in Asparagus, see Fukuda et al. (2005b) and Kubota et al. (2011); subgenus Myrsiphyllum, at least, is probably paraphyletic. Norup et al. (2015) found six main clades within Asparagus as well as two small clades, but relationships between these groups were not well supported.

Previous Relationships. Hemiphylacus used to be placed in Asphodelaceae-Asphodeloideae.

7. Nolinoideae Burnett   Back to Asparagales


Herbs, rhizomatous or not, to climbers, shrubs or stout little-branched trees; flavonols, (azetidine-2-carboxylic acid [non-protein amino acid]), (indolizidine alkaloids), (cardiac glycosides/cardenolides - Convallaria), saponins +; (monocot secondary thickening +); (velamen +); (vessel elements in roots with simple perforation plates; vessels in stem - many ruscoids); (vascular bundles amphivasal); also styloids +; cuticular wax rodlets parallel; leaves (scarious), spiral or two-ranked (opposite, whorled, esp. Polygonatum), (blade broad, venation reticulate), margins spiny or not, (petiolate; leaf base not sheathing); (inflorescence also cymose); (flowers 2-merous - some Maianthemum, Aspidistra); T not connate, (2-13, corona + [Aspidistra]), (with three traces - Smilacina); (A 2-24), (adnate to base of tube), (connate); pollen often inaperturate/diffuse sulcate; stigma (much expanded and fungiform), wet; ovules 1-6(-many)/carpel, (micropyle bi-, endostomal), outer integument 2-8 cells across, parietal tissue 1-3(-4) cells across, (0, but lateral tissue), nucellar cap 0 (+), obturator [funicle or ovary wall] +/0, (chalazal vascular bundle branched), raphides +/0; (embryo sac bisporic, 8 nucleate [Allium type]; tetrasporic, 16-nucleate [Drusa type]), (antipodal cells numerous, persistent), (embryo sac haustorium - Dasylirion); (fruit ± a drupe); seeds rounded (angled), (sarcotesta - Ophiopogoneae), (testa 0 - Dracaena), phytomelan 0, (phlobaphene +); (endosperm nuclear); n = 5-7, 9, 17, 18-21, chromosomes 0.5-19 µm long (bimodal); cotyledon not photosynthetic, (coleoptile +), primary root well developed, branched or not.

26[list]/505: Dracaena (170), Aspidistra (135), Eriospermum (100), Polygonatum (60), Ophiopogon (55). N. hemisphere, esp. Southeast Asia-Malesia (Convallariaceae s. str.), Europe and the Near East (Ruscaceae s. str.), S.W. North America (Nolinaceae s. str.), Africa, esp. the Cape and S.W. (Eriospermaceae s. str.) (map: from Meusel et al. 1965; Hultén & Fries 1986; Perry 1994, incomplete). [Photo - Ruscus Flower, Eriospermum Flower, © M. Elvin.]

Age. Divergence within Nolinoideae began (53-)41(-31) or ca 23.6 m.y.a. (S. Chen et al. 2013).

Synonymy: Aspidistraceae Hasskarl, Convallariaceae Horaninow, Dracaenaceae Salisbury, Eriospermaceae d'Orbigny, Nolinaceae Nakai, Ophiopogonaceae Meissner, Peliosanthaceae Salisbury, Polygonataceae Salisbury, Ruscaceae M. Roemer, nom. cons., Sansevieraceae Nakai, Tupistraceae Schnizlein

Evolution. Divergence & Distribution. Biogeographical relationships in the the Dracaena group are of considerable interest. Pleomele (= Chrysodracon) from Hawaii is sister to the rest (e.g. Lu & Morden 2010, 2013, 2014), which raises all sorts of biogeographical questions (shades of Hillebrandia?), and in turn Central American species are sister to the remainder. There seems to have been extensive dispersal (and extinction) in this whole clade (Lu & Morden 2014). Lu and Morden (2014) noted several independent transitions to the arborescent habit (perhaps four times) and the development of cylindrical leaves (ca seven times).

Pollination Biology & Seed Dispersal. The flowers of Aspidistra, sometimes borne beneath the litter, often have a large, fungiform stigma, the anthers being hidden below it (Endress 1995b: floral morphology), or the anthers converge towards the centre of the flower; in both cases easy access to the nectar is apparently blocked. It has been suggested that such flowers are pollinated by amphipods (Conran & Bradbury 2007 and references), fungus gnats, the phorid fly Megaselia (Vislobokov et al. 2013), or non-galling cecidomyiid midges (Cecidomyiidae, undetermined genus) which also lay eggs in the anthers, the larvae eating the pollen (Vislobokov et al. 2014b). Flowers of some species of Aspidistra look rather those of some Aristolochiaceae or Burmanniaceae, while other species have more conventional sub-rotate flowers with the stamens and stigma/style grouped in the centre, or they have a short corona at the apex of the perianth tube, while yet others have a balloon-like perianth with a little opening at the apex. There may be anything from two to a dozen or more tepal lobes (see also Hou et al. 2009; Li 2004; Vislobokov et al. 2014a). A remarkable and speciose genus; new species are being described at quite a rate

Vegetative Variation. Vegetative variation is particularly impressive. Dracaeana is the only monocot known with a monocot cambium in its roots (Carlquist 2012a). Nolina (ex Nolinaceae) has secondary growth in the stem and is tree-like, Beaucarnea, also tree-like, has a much swollen stem base, while the initiation of the vascular system in the rhizome of Ophiopogon is similar to that in palm stems (Pizzolato 2009).

The leaf blades of some species of Eriospermum have the most remarkable enations on the upper surface. These include fungiform protrusions on the small, crisped, ovate and fleshy blade (E. titanopsoides), a much-branched structure to 12 x 7.5 cm on a much smaller blade (E. ramosum), a bundle of enations with stellate hairs (E. dregei), and paired enations that look as if they should grace the helmets of the Valkyries (E. alcicorne: see Perry 1994 for more details). These may be adaptations for catching water from fog in the arid coastal regions of southwest Africa where they grow (Vogel & Müller-Doblies 2011). Classical morphology suggests that the fleshy leaf of Sansevieria (= Dracaena) develops from the leaf base, the apical portion of the leaf being represented by a Vorlaüferspitze (e.g. Kaplan 1997, vol. 2: chap. 16); depending on the species, the leaf can be developed predominantly from the base (and is flattened) or from the apex (and is terete: Kaplan 1973). Many other taxa, including Maianthemum, have more or less broadly elliptic leaf blades.

Ruscus and its immediate relatives have cladodes, the flowers being born in the middle of a tough, more or less elliptical leaf-like structure. The prophylls are lateral or in some interpretations completely adnate to the axillary shoot, together they form an expanded cladode (Arber 1924a, 1930), or they are homeotic structures (Cooney-Sovetts & Sattler 1987). In any event, the leaves proper are small and scarious and subtend the cladode-like structures (c.f. Asparagus above).

Chemistry, Morphology, etc. Convallarieae are monopodial. Dracaena and relatives have resin canals.

Peliosanthes teta, the only species in the genus, has an ovary that varies from superior to inferior (Jessop 1976: some recognise more species in the genus). The absence of septal nectaries in some Nolinoideae may be connected with the presence of prominent ovary wall obturators; the latter are possibly derived from the former. In Liriope, etc. (Ophiopogoneae), the seeds, with their fleshy testa, are exposed early in development, so they are semi-gymnospermous.

Additional information can be found in Bos (1998: Dracaenaceae), Conran and Tamura (1998: Convallariaceae), Bogler (1998: Nolinaceae), Duthie (1940), Dahlgren (in Dahlgren & Van Wyk 1988) and Terry and Rudall (1998) all Eriospermum, Yeo (1998: Ruscaceae), Judd et al. (2002: general), Judd (2003: Ruscaceae S.E. U.S.A.), Rudall & Campbell (1999: floral morphology), van der Ham (1994: distinctive pollen of Peliosanthes), Stenar (1934, 1953) and Wunderlich (1950), all embryology, Björnstad (1970), Lu (1985), Tillich (1995: seed, etc.), Yamashita and Tamura (2004: chromosomes in Convallarieae) and G.-Y. Wang et al. (2013: chromosomes in Ophiopogoneae).

Phylogeny The placement of Eriospermum (for which, see Perry 1994) as sister to Asparagoideae has quite strong support (Seberg et el. 2012); it and and the very distinct Comospermum are likely to be sister to the rest of the family; both have capsules and hairy seeds. Note, however, that the hairs on the seeds of the two genera develop in different ways, and Comospermum has two tenuinucellate apotropous ovules/carpel, n = 20 vs. n = 7, etc.; the two genera would at first sight seem to be unrelated (Rudall 1999). The poorly understood Peliosanthes may then be sister to the rest of the family (molecular data alone, e.g. Jang & Pfosser 2002). However, G.-Y. Wang et al. (2014) suggest that it is a member of Ophiopogoneae, a group in which capsules open precociously before the seeds are mature. None of these genera was even sub-basal in the study of Seberg et al. (2012), Eriospermum even linking with Asparagoideae.

Relationships within other Nolinoideae are poorly resolved, although major clades largely correspond with tribes (see Conran & Tamura 1998). However, Convallarieae may be paraphyletic with Aspidistreae and Ruscus and relatives embedded (Yamashita & Tamura 2000: Eriospermum not included; Rudall et al. 2000b); in Ruscus and immediate relatives a mitochondral cox2 intron is missing (Kudla et al. 2002). Meng et al. (2014) discussed relationships within Polygonatum and its relatives (Polygonateae). For relationships of ex-Nolinaceae, -Dracaenaceae, etc., see also Bogler and Simpson (1996). Dracaena can be circumscribed to include most of Pleomele and Sanseviera, with Pleomele from Hawaii (= Chrysodracon) sister to the whole of the rest of the group (e.g. Lu & Morden 2010, 2013, 2014; c.f. Baldwin & Webb 2016); this clade may be sister to Ruscus and relatives. Rojas-Piña et al. (2014) evaluate relationships around Beaucarnea and Nolina; there are three morphologically distinctive clades of tree-like plants there, although support for the monophyly of Nolina is not strong.

Classification. There has been debate over the generic limits of Maianthemum which includes Smilacina here. A broad circumscription is appropriate aince there is little support for groupings within the combined group, but the whole clade is well supported as being monophyletic (Kim & Lee 2007; Meng et al. 2008).