EMBRYOPSIDA Pirani & Prado
Gametophyte dominant, independent, multicellular, not motile, initially ±globular; showing gravitropism; acquisition of phenylalanine lysase [PAL], microbial terpene synthase-like genes +, triterpenoids produced by CYP716 enzymes, phenylpropanoid metabolism [lignans +, flavonoids + (absorbtion of UV radiation)], xyloglucans in primary cell wall, side chains charged; plant poikilohydrous [protoplasm dessication tolerant], ectohydrous [free water outside plant physiologically important]; thalloid, leafy, with single-celled apical meristem, tissues little differentiated, rhizoids +, unicellular; chloroplasts several per cell, pyrenoids 0; glycolate metabolism in leaf peroxisomes [glyoxysomes]; centrioles/centrosomes in vegetative cells 0, microtubules with γ-tubulin along their lengths [?here], interphase microtubules form hoop-like system; metaphase spindle anastral, predictive preprophase band + [with microtubules and F-actin; where new cell wall will form], phragmoplast + [cell wall deposition centrifugal, from around the anaphase spindle], plasmodesmata +; antheridia and archegonia jacketed, surficial; blepharoplast +, centrioles develop de novo, bicentriole pair coaxial, separate at midpoint, centrioles rotate, associated with basal bodies of cilia, multilayered structure + [4 layers: L1, L4, tubules; L2, L3, short vertical lamellae] (0), spline + [tubules from L1 encircling spermatid], basal body 200-250 nm long, associated with amorphous electron-dense material, microtubules in basal end lacking symmetry, stellate array of filaments in transition zone extended, axonemal cap 0 [microtubules disorganized at apex of cilium]; male gametes [spermatozoids] with a left-handed coil, cilia 2, lateral; oogamy; sporophyte multicellular, cuticle +, plane of first cell division transverse [with respect to long axis of archegonium/embryo sac], sporangium and upper part of seta developing from epibasal cell [towards the archegonial neck, exoscopic], with at least transient apical cell [?level], initially surrounded by and dependent on gametophyte, placental transfer cells +, in both sporophyte and gametophyte, wall ingrowths develop early; suspensor/foot +, cells at foot tip somewhat haustorial; sporangium +, single, terminal, dehiscence longitudinal; meiosis sporic, monoplastidic, MTOC [MTOC = microtubule organizing centre] associated with plastid, sporocytes 4-lobed, cytokinesis simultaneous, preceding nuclear division, quadripolar microtubule system +; wall development both centripetal and centrifugal, 1000 spores/sporangium, sporopollenin in the spore wall laid down in association with trilamellar layers [white-line centred lamellae; tripartite lamellae]; nuclear genome size [1C] <1.4 pg, main telomere sequence motif TTTAGGG, LEAFY and KNOX1 and KNOX2 genes present, ethylene involved in cell elongation; chloroplast genome with close association between trnLUAA and trnFGAA genes [precursors for starch synthesis], tufA gene moved to nucleus; mitochondrial trnS(gcu) and trnN(guu) genes +.
Many of the bolded characters in the characterization above are apomorphies of subsets of streptophytes along the lineage leading to the embryophytes, not apomorphies of crown-group embryophytes per se.
All groups below are crown groups, nearly all are extant. Characters mentioned are those of the immediate common ancestor of the group,  contains explanatory material, () features common in clade, exact status unclear.
Abscisic acid, L- and D-methionine distinguished metabolically; pro- and metaphase spindles acentric; sporophyte with polar transport of auxins, class 1 KNOX genes expressed in sporangium alone; sporangium wall 4≤ cells across [≡ eusporangium], tapetum +, secreting sporopollenin, which obscures outer white-line centred lamellae, columella +, developing from endothecial cells; stomata +, on sporangium, anomocytic, cell lineage that produces them with symmetric divisions [perigenous]; underlying similarities in the development of conducting tissue and of rhizoids/root hairs; spores trilete; shoot meristem patterning gene families expressed; MIKC, MI*K*C* genes, post-transcriptional editing of chloroplast genes; gain of three group II mitochondrial introns, mitochondrial trnS(gcu) and trnN(guu) genes 0.
[Anthocerophyta + Polysporangiophyta]: gametophyte leafless; archegonia embedded/sunken [only neck protruding]; sporophyte long-lived, chlorophyllous; cell walls with xylans.
Sporophyte well developed, branched, branching apical, dichotomous, potentially indeterminate; hydroids +; stomata on stem; sporangia several, terminal; spore walls not multilamellate [?here].
Vascular tissue + [tracheids, walls with bars of secondary thickening].
EXTANT TRACHEOPHYTA / VASCULAR PLANTS
Sporophyte with photosynthetic red light response, stomata open in response to blue light; plant homoiohydrous [water content of protoplasm relatively stable]; control of leaf hydration passive; plant endohydrous [physiologically important free water inside plant]; (condensed or nonhydrolyzable tannins/proanthocyanidins +); xyloglucans with side chains uncharged [?level], in secondary walls of vascular and mechanical tissue; lignins +; stem apex multicellular, with cytohistochemical zonation, plasmodesmata formation based on cell lineage; tracheids +, in both protoxylem and metaxylem, G- and S-types; sieve cells + [nucleus degenerating]; endodermis +; leaves/sporophylls spirally arranged, blades with mean venation density ca 1.8 mm/mm2 [to 5 mm/mm2], all epidermal cells with chloroplasts; sporangia adaxial, columella 0; tapetum glandular; ?position of transfer cells; MTOCs not associated with plastids, basal body 350-550 nm long, stellate array in transition region initially joining microtubule triplets; suspensor +, shoot apex developing away from micropyle/archegonial neck [from hypobasal cell, endoscopic], root lateral with respect to the longitudinal axis of the embryo [plant homorhizic].[MONILOPHYTA + LIGNOPHYTA]
Sporophyte endomycorrhizal [with Glomeromycota]; growth ± monopodial, branching spiral; roots +, endogenous, positively geotropic, root hairs and root cap +, protoxylem exarch, lateral roots +, endogenous; G-type tracheids +, with scalariform-bordered pits; leaves with apical/marginal growth, venation development basipetal, growth determinate; sporangium dehiscence by a single longitudinal slit; cells polyplastidic, MTOCs diffuse, perinuclear, migratory; blepharoplasts +, paired, with electron-dense material, centrioles on periphery, male gametes multiciliate; chloroplast long single copy ca 30kb inversion [from psbM to ycf2]; mitochondrion with loss of 4 genes, absence of numerous group II introns; LITTLE ZIPPER proteins.
Sporophyte woody; stem branching lateral, meristems axillary; lateral root origin from the pericycle; cork cambium + [producing cork abaxially], vascular cambium bifacial [producing phloem abaxially and xylem adaxially].
Plants heterosporous; megasporangium surrounded by cupule [i.e. = unitegmic ovule, cupule = integument]; pollen lands on ovule; megaspore germination endosporic [female gametophyte initially retained on the plant].
EXTANT SEED PLANTS / SPERMATOPHYTA
Plant evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); microbial terpene synthase-like genes 0; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignin chains started by monolignol dimerization [resinols common], particularly with guaiacyl and p-hydroxyphenyl [G + H] units [sinapyl units uncommon, no Maüle reaction]; root stele diarch to pentarch, xylem and phloem originating on alternating radii, cork cambium deep seated; stem apical meristem complex [with quiescent centre, etc.], plasmodesma density in SAM 1.6-6.2[mean]/μm2 [interface-specific plasmodesmatal network]; eustele +, protoxylem endarch, endodermis 0; wood homoxylous, tracheids and rays alone, tracheid/tracheid pits circular, bordered; mature sieve tube/cell lacking functioning nucleus, sieve tube plastids with starch grains; phloem fibres +; cork cambium superficial; leaf nodes 1:1, a single trace leaving the vascular sympodium; leaf vascular bundles amphicribral; guard cells the only epidermal cells with chloroplasts, stomatal pore with active opening in response to leaf hydration, control by abscisic acid, metabolic regulation of water use efficiency, etc.; axillary buds +, exogenous; prophylls two, lateral; leaves with petiole and lamina, development basipetal, lamina simple; sporangia borne on sporophylls; spores not dormant; microsporophylls aggregated in indeterminate cones/strobili; grains monosulcate, aperture in ana- position [distal], primexine + [involved in exine pattern formation with deposition of sporopollenin from tapetum there], exine and intine homogeneous, exine alveolar/honeycomb; ovules with parietal tissue [= crassinucellate], megaspore tetrad linear, functional megaspore single, chalazal, sporopollenin 0; gametophyte ± wholly dependent on sporophyte, development initially endosporic [apical cell 0, rhizoids 0, etc.]; male gametophyte with tube developing from distal end of grain, male gametes two, developing after pollination, with cell walls; female gametophyte initially syncytial, walls then surrounding individual nuclei; embryo cellular ab initio, suspensor short-minute, embryonic axis straight [shoot and root at opposite ends; plant allorhizic], cotyledons 2; embryo ± dormant; chloroplast ycf2 gene in inverted repeat, trans splicing of five mitochondrial group II introns, rpl6 gene absent; whole nuclear genome duplication [ζ - zeta - duplication], two copies of LEAFY gene, PHY gene duplications [three - [BP [A/N + C/O]] - copies], 5.8S and 5S rDNA in separate clusters.
ANGIOSPERMAE / MAGNOLIOPHYTA
Lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, apigenin and/or luteolin scattered, [cyanogenesis in ANA grade?], lignin also with syringyl units common [G + S lignin, positive Maüle reaction - syringyl:guaiacyl ratio more than 2-2.5:1], hemicelluloses as xyloglucans; root cap meristem closed (open); pith relatively inconspicuous, lateral roots initiated immediately to the side of [when diarch] or opposite xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0, hypodermis suberised and with Casparian strip [= exodermis]; shoot apex with tunica-corpus construction, tunica 2-layered; starch grains simple; primary cell wall mostly with pectic polysaccharides, poor in mannans; tracheid:tracheid [end wall] plates with scalariform pitting, wood parenchyma +; sieve tubes enucleate, sieve plate with pores (0.1-)0.5-10< µm across, cytoplasm with P-proteins, not occluding pores of plate, companion cell and sieve tube from same mother cell; ?phloem loading/sugar transport; nodes 1:?; dark reversal Pfr → Pr; protoplasm dessication tolerant [plant poikilohydric]; stomata brachyparacytic [ends of subsidiary cells level with ends of pore], outer stomatal ledges producing vestibule, reduction in stomatal conductance with increasing CO2 concentration; lamina formed from the primordial leaf apex, margins toothed, development of venation acropetal, overall growth ± diffuse, secondary veins pinnate, fine venation hierarchical-reticulate, (1.7-)4.1(-5.7) mm/mm2, vein endings free; flowers perfect, pedicellate, ± haplomorphic, protogynous; parts free, numbers variable, development centripetal; P +, ?insertion, members each with a single trace, outer members not sharply differentiated from the others, not enclosing the floral bud; A many, filament not sharply distinguished from anther, stout, broad, with a single trace, anther introrse, tetrasporangiate, sporangia in two groups of two [dithecal], each theca dehiscing longitudinally by a common slit, ± embedded in the filament, walls with at least outer secondary parietal cells dividing, endothecium +, cells elongated at right angles to long axis of anther; tapetal cells binucleate; microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing; pollen subspherical, tectum continuous or microperforate, ektexine columellate, endexine lamellate only in the apertural regions, thin, compact, intine in apertural areas thick, pollenkitt +; nectary 0; carpels present, superior, free, several, ascidiate [postgenital occlusion by secretion], stylulus at most short [shorter than ovary], hollow, cavity not lined by distinct epidermal layer, stigma ± decurrent, carinal, dry; suprastylar extragynoecial compitum +; ovules few [?1]/carpel, marginal, anatropous, bitegmic, micropyle endostomal, outer integument 2-3 cells across, often largely subdermal in origin, inner integument 2-3 cells across, often dermal in origin, parietal tissue 1-3 cells across, nucellar cap?; megasporocyte single, hypodermal, functional megaspore lacking cuticle; female gametophyte lacking chlorophyll, not photosynthesising, four-celled [one module, nucleus of egg cell sister to one of the polar nuclei]; ovule not increasing in size between pollination and fertilization; pollen grains land on stigma, bicellular at dispersal, mature male gametophyte tricellular, germinating in less than 3 hours, pollen tube elongated, unbranched, growing between cells, growth rate (20-)80-20,000 µm/hour, apex of pectins, wall with callose, lumen with callose plugs, penetration of ovules via micropyle [porogamous], whole process takes ca 18 hours, distance to first ovule 1.1-2.1 mm; male gametes lacking cell walls, ciliae 0, siphonogamy; double fertilization +, ovules aborting unless fertilized; P deciduous in fruit; mature seed much larger than fertilized ovule, small , dry [no sarcotesta], exotestal; endosperm +, cellular, development heteropolar [first division oblique, micropylar end initially with a single large cell, divisions uniseriate, chalazal cell smaller, divisions in several planes], copious, oily and/or proteinaceous, embryo short [<¼ length of seed]; plastid and mitochondrial transmission maternal; Arabidopsis-type telomeres [(TTTAGGG)n]; nuclear genome size [1C] <1.4 pg [mean 1C = 18.1 pg, 1 pg = 109 base pairs], whole nuclear genome duplication [ε/epsilon event]; ndhB gene 21 codons enlarged at the 5' end, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, palaeo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and three copies of the PHY gene, [PHYB [PHYA + PHYC]]; chloroplast chlB, -L, -N, trnP-GGG genes 0.
[NYMPHAEALES [AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]]: wood fibres +; axial parenchyma diffuse or diffuse-in-aggregates; pollen monosulcate [anasulcate], tectum reticulate-perforate [here?]; ?genome duplication; "DEAER" motif in AP3 and PI genes lost, gaps in these genes.
[AUSTROBAILEYALES [[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]]]: phloem loading passive, via symplast, plasmodesmata numerous; vessel elements with scalariform perforation plates in primary xylem; essential oils in specialized cells [lamina and P ± pellucid-punctate]; tension wood + [reaction wood: with gelatinous fibres, G-fibres, on adaxial side of branch/stem junction]; tectum reticulate; anther wall with outer secondary parietal cell layer dividing; nucellar cap + [character lost where in eudicots?]; 12BP [4 amino acids] deletion in P1 gene.
[[CHLORANTHALES + MAGNOLIIDS] [MONOCOTS [CERATOPHYLLALES + EUDICOTS]]] / MESANGIOSPERMAE: benzylisoquinoline alkaloids +; sesquiterpene synthase subfamily a [TPS-a] [?level], polyacetate derived anthraquinones + [?level]; outer epidermal walls of root elongation zone with cellulose fibrils oriented transverse to root axis; P more or less whorled, 3-merous [?here]; pollen tube growth intra-gynoecial; extragynoecial compitum 0; carpels plicate [?here]; embryo sac bipolar, 8 nucleate, antipodal cells persisting; endosperm triploid.
[MONOCOTS [CERATOPHYLLALES + EUDICOTS]]: (extra-floral nectaries +); (veins in lamina often 7-17 mm/mm2 or more [mean for eudicots 8.0]); (stamens opposite [two whorls of] P); (pollen tube growth fast).
[CERATOPHYLLALES + EUDICOTS]: ethereal oils 0.
EUDICOTS: (Myricetin, delphinidin +), asarone 0 [unknown in some groups, + in some asterids]; root epidermis derived from root cap [?Buxaceae, etc.]; (vessel elements with simple perforation plates in primary xylem); nodes 3:3; stomata anomocytic; flowers (dimerous), cyclic; protandry common; K/outer P members with three traces, ("C" +, with a single trace); A ?, filaments fairly slender, anthers basifixed; microsporogenesis simultaneous, pollen tricolpate, apertures in pairs at six points of the young tetrad [Fischer's rule], cleavage centripetal, wall with endexine; G with complete postgenital fusion, stylulus/style solid [?here]; seed coat?
[PROTEALES [TROCHODENDRALES [BUXALES + CORE EUDICOTS]]]: (axial/receptacular nectary +).
[TROCHODENDRALES [BUXALES + CORE EUDICOTS]]: benzylisoquinoline alkaloids 0; euAP3 + TM6 genes [duplication of paleoAP3 gene: B class], mitochondrial rps2 gene lost.
[BUXALES + CORE EUDICOTS]: mitochondrial rps11 gene lost.
CORE EUDICOTS / GUNNERIDAE: (ellagic and gallic acids +); leaf margins serrate; compitum + [one position]; micropyle?; γ whole nuclear genome duplication [palaeohexaploidy, gamma triplication], PI-dB motif +, small deletion in the 18S ribosomal DNA common.
[ROSIDS ET AL. + ASTERIDS ET AL.] / PENTAPETALAE: root apical meristem closed; (cyanogenesis also via [iso]leucine, valine and phenylalanine pathways); flowers rather stereotyped: 5-merous, parts whorled; P = calyx + corolla, the calyx enclosing the flower in bud, sepals with three or more traces, petals with a single trace; stamens = 2x K/C, in two whorls, internal/adaxial to the corolla whorl, alternating, (numerous, but then usually fasciculate and/or centrifugal); pollen tricolporate; G , G  also common, when [G 2], carpels superposed, placentation axile, style +, stigma not decurrent; compitum +; endosperm nuclear; fruit dry, dehiscent, loculicidal [when a capsule]; RNase-based gametophytic incompatibility system present; floral nectaries with CRABSCLAW expression; (monosymmetric flowers with adaxial/dorsal CYC expression).
[DILLENIALES [SAXIFRAGALES [VITALES + ROSIDS s. str.]]]: stipules + [usually apparently inserted on the stem].
[SAXIFRAGALES [VITALES + ROSIDS]] / ROSANAE Takhtajan / SUPERROSIDAE: ??
[VITALES + ROSIDS] / ROSIDAE: anthers ± dorsifixed, transition to filament narrow, connective thin.
ROSIDS: (mucilage cells with thickened inner periclinal walls and distinct cytoplasm); if nectary +, usu. receptacular; embryo long; chloroplast infA gene defunct, mitochondrial coxII.i3 intron 0.
ROSID I / FABIDAE / [ZYGOPHYLLALES [the COM clade + the nitrogen-fixing clade]]: endosperm scanty.
[the COM clade + the nitrogen-fixing clade]: ?
[FABALES [ROSALES [CUCURBITALES + FAGALES]]] / the nitrogen-fixing clade / fabids: (N-fixing by associated root-dwelling bacteria); tension wood +; seed exotestal.
[ROSALES [CUCURBITALES + FAGALES]]: (actinomycete Frankia infection +); styles separate; ovules 1-2/carpel, apical.
[CUCURBITALES + FAGALES]: P parts similar; ovary inferior; fruit 1-seeded, indehiscent.
FAGALES Engler Main Tree.
Plant ectomycorrhizal; (Frankia infection +, by root hairs); (flavonols), dihydroflavonols, ellagic acid +; (cork cambium outer cortical); vessel elements also with scalariform perforation plates; sieve tubes with non-dispersive P-protein bodies; buds perulate; lamina margins toothed, secondary veins proceeding straight to teeth, teeth not glandular, with higher-order veins convergent on them [= urticoid]; plants monoecious, inflorescence with compact cymose clusters of flowers, flowers very small, (± monosymmetric by reduction), sessile; P +, uniseriate; nectary 0; staminate flowers: inflorescence a catkin; A opposite P; pollen oblate, thickened sexine arches going from pore to pore, visible as bands [arci], cavity between inner and outer pores [vestibulum], tectum ± spinulate, infratectum granular; carpellate flowers: style undivided, ± 0, stigma ± decurrent, linear, dry; ovule 2/carpel, pendulous, epitropous, unitegmic; megaspore mother cells several; ovules poorly developed at pollination, fertilization delayed; fruits dry, nut-like [= nuts]; testa vascularized, not mechanical, exotesta often enlarged and persisting; cotyledons large. - 7 families, 33 genera, 1,055 species.
Age. Ages for crown-group Fagales suggested by Cook and Crisp (2005) are 95-75 m.y. and by Xiang et al. (2014) rather older, (107.3-)105.2(-101.3) m.y., while Sauquet et al. (2011) give a range of dates from (124.8-)120.2-67.3(-48.9) m.y. and Xing et al. (2014) suggest ages of 125-91.8 m. years; at around 92 m.y. the dates in Larson-Johnson (2015) fit with most of these. Ages of (106.5-)104.9, 104.1(-99.9) m.y. in H.-L. Li et al. (2015) show little spread, while the youngest dates, at around 68.6-62.2 m.y.a., are those of Xue et al. (2012), and of ca 61 m.y., that of Quirk et al. (2012). Other dates: ca 82.3 m.y. (Tank et al. 2015: Table S2).
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. From the rich fossil record of Fagales, Friis et al. (2006a) suggested that all major fagalean lineages were present at the latest by the Cenomanian (early Late Cretaceous), ca 97 m.y.a., and fagalean leaf fossils are reported from Queensland, Australia then - at that time, Australia had barely separated from Antarctica (e.g. McLoughlin et al. 1995). Xiang et al. (2014) discuss diversification of the order in considerable detail, emphasising the distinction between wind- (most species of Fagus were included here) versus animal-dispersed fruits and the closed habitats preferred by the former group of species and the open habitats preferred by the latter group; they also detected a number of shifts in diversification rates. Larson-Johnson (2015) integrated fossils with fruits in a study of fruit evolution and diversification patterns in the order.
The morphologies of flowers of some Cretaceous fossil taxa assigned in or near Fagales are substantially different from those of extant members. Thus there are suggestions of nectary lobes between the stamens in the staminate and perfect flowers of Antiquacupula and the inner walls of the fruit loculi are glabrous; the flowers are staminate and perfect and have a floral formula of P 3 + 3; A 12, dorsifixed; nectaries +, G 3, inferior (Sims et al. 1998; Herendeen et al. 1999). Archaefagacea has a tricarpellate gynoecium, two ovules per carpel and sometimes three-seeded fruits. Unnamed fossils from Massachusetts have a character combination of flowers perfect, P 6, A 12, adnate to P, nectaries, inferior ovary with ovules mature at time of pollination, and single-seeded and very small fruits that are just possibly dehiscent (Taylor et al. 2012). If they belong to stem Fagales, single-seeded fruits may have evolved before wind pollination; the very small size of the seeds/fruits (<2 mm long) is consistent with the age of the fossils, ca 75 m.y. in the Campanian, since flowers then tended to be small (Taylor et al. 2012). Taylor et al. (2012) suggested that the members of the uniseriate perianth might be connate via hairs, but note that the perianth bases are very small, in this respect being rather unlike sepals in the rosids. For fossils, see especially Friis et al. (2011) and Larson-Johnson (2015), the latter placing a number of fossils with fruits on a phylogenetic tree of the order (see the supplementary material for a critical evaluation of the fossil material, ages of fossils assigned to extant genera, data matrix, etc.).
Where change in infratectum structure is to be placed on the tree seems unclear when treated at the family level; either one gain, an ordinal apomorphy, and one reversion (Fagaceae), or two gains (see also Doyle 2009). For the evolution of the foot layer, see Denk and Tekleva (2014); the ancestral state for Fagaceae - foot layer thick, regular - should be pegged to this node, but I do not know variation in the foot layer above Fagaceae. Schönenberger et al. (2001b) and Friis et al. (2003a) give useful tables comparing the morphology of extant and fossil members of Fagales; see also Crepet et al. (2008), Takahashi et al. (2008a) and Taylor et al. (2012: some outgroups). For fossils producing Normapolles pollen, see below.
Ecology & Physiology. Fagales are the largest clade of extant seed-plants in which ectomycorrhizal (ECM) associations are pervasive. Nevertheless, although they are hardly particularly speciose (e.g. Magallón & Sanderson 2001), members, especially Fagaceae, can dominate the forests in which they grow, and this is discussed further in Clade Asymmetries, while ECM associations plant-fungal associations in general are discussed. The order is particularly well represented in forests in temperate and tropical montane regions and the climatic preferences for the immediate ancestor of the order may have been for more or less warm and aseasonal temperate conditions.
For nitrogen fixation by Frankia, see elsewhere.
Pollination Biology & Seed Dispersal. Wind pollination and monoecy pervade the order, although taxa like Lithocarpus are pollinated by insects, and insect pollination may have occurred in some fossil taxa, too. Delayed fertilization, intermittent pollen tube growth (e.g. Sogo & Tobe 2005, 2006a, b, d [the last for a summary]), and chalazogamy (see e.g. Benson 1894; Nawashin 1899; Swamy 1948b and references) are also common, however, chalazogamy may not be plesiomorphic in the order. (Fertilization in Nothofagaceae is unknown and both Fagaceae and Myricaceae are porogamous.) Delayed fertilization, which also occurs in Fagaceae, is associated with the immaturity of the ovules at pollination and competition between the ovules and sometimes between the several embryo sacs that develop within the one ovule (see Sogo & Tobe 2005d). The immaturity of the ovules can be extreme, thus in Corylus avellana the ovules do not even begin to develop until after pollination (Germain 1994).
Fruits throughout the order are single-seeded, as is very common in wind-pollinated plants, whatever the number of ovules in the young ovary - note, however, this feature may be an apomorphy for [Fagales + Cucurbitales]. See Tiffney (1986a) and especially Larson-Johnson (2015) for the evolution of fruits in Fagales. The order has wind- or animal-dispersed propagules, the former perhaps being the plesiomorphic condition (Larson-Johnson 2015: immediate outgroups not necessarily so), while within Fagales there have been around seven transitions to biotic dispersal and four to abiotic dispersal, three of the latter being reversals. An increase in diversification rates is associated with the adoption of animal-dispersal, and scatter-hoarding by jays and small rodents is most commonly involved (Larson-Johnson 2015).
Plant-Animal Interactions. Interestingly, larvae of both Heterobathmiidae (the adults have jaws) and Eriocraniidae (Glossata, with proboscis and jaws), the two basal clades in the lepidopteran Angiospermivora, are found as leaf miners on Fagales, on Nothofagaceae and on Fagaceae and Betulaceae (also Rosaceae) respectively (Shields 1988; Imada et al. 2011; Regier et al. 2015). Phyllonorycter leaf-mining moths (members of the fairly basal glossatan microlepidopteran Gracillariidae-Phyllocnistinae) are also especially speciose, with about half the known host records being on members of Fagales (Lopez-Vaamonde et al. 2003; see also Regier et al. 2013). Diversification of the moth clade seems to have occurred about 50.8-27.3 m.y.a., well after that of Fagales (see above) although the origination of the clade was some 76.3-50.3 m.y.a. (Lopez-Vaamonde et al. 2006). Lycaenidae caterpillars are also quite commonly to be found on members of Fagales (see Fiedler 1991).
Bacterial/Fungal Associations. ECM Agaricales are common on Fagales, and the crown group origins of the 10 or so clades involved are split almost equally between Late Cretaceous and Eocene (Ryberg & Matheny 2012). However, the relative timing of diversification of the ECM fungi and of Fagales is unclear. In Boletales, at least, ECM fungi may have evolved from brown rot fungi in the ecological context of soils low in nitrogen (and high in organic material) formed by the activities of these fungi. Dates of origin of ECM associations there - which happened more than once - are also late Cretaceous and younger (Eastwood et al. 2011). Sebacinales-Sebacinaceae are other ECM fungi commonly associated with Fagales (Weiß et al. 2016). Some ECM fungi form tuberculate structures on the roots (Smith & Pfister 2009). AM associations are less common, but it is interesting that they have been found in the groups that are known to fix nitrogen (Rose 1980).
Rusts on Fagales are predominantly members of Pucciniastraceae, a group also to be found on ferns (Savile 1979).
Associations with nitrogen-fixing bacteria are sporadic. One Frankia clade involved in nitrogen fixation is restricted to Fagales, although members of another clade are also to be found here (Clawson et al. 2004). For a summary of what is known about nitrogen fixation, see Santi et al. (2013), for stem-group ages of N-fixing clades, Late Cretaceous, see H.-L. Li et al. (2015), and for more details on the Frankia-Angiosperm association,
Chemistry, Morphology, etc. Although the tepals in Fagales are small, they may have three traces, and petals with three traces are also found in some fossil taxa. Carpel orientation and integument number are variable. Ovule structure is unclear in part because of the great development of megaspore mother cell tissue in some taxa and the relation of these mother cells to the cells of the mature embryo sac. Taylor et al. (2012) suggested that an ovule that is straight when young, becoming curved only later, might be a distinctive feature of the order. Germination is often both hypogeal and epigeal in the one family.
For chemistry, see Giannasi (1986); for cork cambium initiation, see Weiss (1890); vegetative morphology, see Hickey and Taylor (1991); flower and inflorescence morphology, see Abbe (1974); pollen, see Zavada and Dilcher (1986), Feuer (1991) and especially Friis et al. (2006a); embryology, Benson (1894) and Xing et al. (1998); and for fruit wall anatomy, see Soepadmo (1967b).
Phylogeny. Relationships within Fagales are fairly well resolved, although the position of Myricaceae remains uncertain. Manos and Steele (1997) placed Myrica as sister to [Casuarinaceae [Ticodendraceae + Betulaceae]], in a matK and combined matK + rbcL analysis, although support was weak (see also Sauquet et al. 2012: 67% bootstrap support), but sister to all Fagales except Nothofagaceae and Fagaceae in a rbcL analysis, the latter set of relationships also being found by R.-Q. Li et al. (2002: only 61% bootstrap support) using trnL-F sequence data. Cook and Crisp (2005) found the relationships [Juglandaceae [Myricaceae [Casuarinaceae + Betulaceae]]]. R.-Q. Li et al. (2004: six genes, all three genomes) found Myricaceae to be sister to Juglandaceae, although still support was not strong, as did Herbert et al. (2006: three genes, little support for the position of Myricaceae); support was, however, good in the Bayesian analysis of Soltis et al. (2007a: sampling poor; see also Larson-Johnson 2015: support not strong; H.-L. Li et al. 2016). A recent comprehensive five-locus chloroplast phylogeny of Fagales has not changed the situation, and although there was some support for a [Juglandaceae [Myricaceae + The Rest]] clade, it was not strong (Xiang et al. 2014) and that topology was also recovered by Xing et al. (2014), H.-L. Li et al. (2015) and M. Sun et al. (2016) and Z.-D. Chen et al. (2016), the last two including details of infrafamilial relationships.
Previous Relationships. Fagales are the core of the old "Englerian" Amentiferae which have since been comprehensively demolished; a somewhat larger group, Juliflorae, included all broad-leaved angiosperms with very reduced flowers, so including Platanaceae, Lacistemaceae, Chloranthaceae, Piperaceae, etc. (e.g. Eichler 1878). Its members have since found resting places among many otherwise entirely unrelated groups within eudicots such as Malpighiales (Salicaceae), Proteales (Platanaceae), and Rosales (Ulmaceae and relatives: e.g. Qiu et al. 1998), and in or near the magnoliids (Piperaceae, Chloranthaceae respectively). They also included Eupteleaceae (Ranunculales), Myrothamnaceae (core eudicot), Eucommiaceae (Garryales, a lamiid), and the like. In the late nineteenth and early twentieth centuries in particular, a number of botanists thought that Amentiferae were primitive, and the chalazogamy common in the order was thought to be intermediate between fertilization in some gymosperms and the porogamy of most angiosperms (e.g. Nawaschin 1895). Hamamelid taxa such as Altingiaceae and Hamamelidaceae were thought to be intermediate between Amentiferae and more conventional broad-leaved angiosperms, but they, too, are not related to Fagales (see Saxifragales here).
Fagales comprise the Faganae and two and a half more superorders in Takhtajan (1997).
Includes Betulaceae, Casuarinaceae, Fagaceae, Juglandaceae, Myricaceae, Nothofagaceae, Ticodendraceae.
Synonymy: Juglandineae Thorne & Reveal, Myricineae Thorne & Reveal - Betulales Martius, Carpinales Döll, Casuarinales Berchtold & J. Presl, Corylales Dumortier, Juglandales Berchtold & J. Presl, Myricales Martius, Nothofagales Doweld, Quercales Burnett, Rhoipteleales Reveal - Casuarinanae Reveal & Doweld, Faganae Takhtajan, Juglandanae Reveal
NOTHOFAGACEAE Kuprianova Back to Fagales
(Plant deciduous); chemistry?; sclereid nests?; peltate glandular hairs +; perulae decussate; leaves two-ranked (spiral), lamina (punctate), vernation various, margins also entire, stipules usu. peltate, enclosing colleters; P uniseriate; staminate flowers: P connate; A 10-15(-many), basifixed, connective usu. produced; pollen 3-10 colpate, ± oblate, aperture margins raised, surface warty-granular to spinulose, exine infratectum granular; pistillode 0; carpellate flowers: 1-3 together; (staminodes +); G [2-3], median member abaxial; ovule integument 4-7 cells across, parietal tissue ?1-2 cells across, nucellar cap 0, supra-chalazal tissue massive, postament +, flat-topped, large; megaspore mother cells?; fertilization?; cupule +, 2-(3-)4-valved, lamellate, nuts (1-)3(-7)/cupule, angled [lenticular (central) or triangular], wall with transversely elongated sclereids in middle; testa?; endosperm nuclear, 0, cotyledons folded; n = 13; ?germination.
1[list]/35. New Guinea to South America (map: from Good 1974, slightly modified; green, Cretaceous to Mid-Caenozoic fossils [also in Australia, New Zealand and South America where the genus is currently found], from Dettmann et al. 1990). [Photo - Branch.]
Age. Cook and Crisp (2005) estimated the age of crown group Nothofagaceae at only (66-)58-ca. 43(-ca 35[?-21]) m.y., i.e., decidedly after the first fossil records (see below), while Heads (2006), accepting the identity of those fossils, saw an age of around 72 m.y. at least. Sauquet et al. (2012) used a variety of calibrations and obtained ages ranged from (113.6-)100.3-23.5(-13.3) m.y., while (77-)76.7(-75.2) m.y. is the estimate in Xiang et al. (2014). Crown and stem ages of 36 and 61 m.y.a. respectively were suggested by Quirk et al. (2012).
Fossils identified as belonging to all four subgenera are known from the Late Campanian 73-71 m.y.a. in Antarctica (Dettmann et al. 1990; Swenson et al. 2001; Cantrill & Poole 2005) and Nothofagus-like pollen (Nothofagites) characterized southern temperate Gondwanan areas during the later Cretaceous (Nichols & Johnson 2008). Given such dates, the pollen types must have evolved in parallel (Cook & Crisp 2005), or the pollen has been misinterpreted, or some molecular age estimates are incorrect.
Evolution: Divergence & Distribution. Bouchenak-Khelladi et al. (2015) suggested that there was a slow-down in diversification rate here.
The biogeography of Nothofagus has been much discussed. The general pattern of diversification in the genus is the "broom and handle" type (Cook & Crisp 2005); either persistence of a not very speciose lineage, or diversification followed by near-extinction and then diversification again. But is the current distribution caused by continental drift, with the massings of species seen today relecting ancestral massings (Heads 2006)? Here global vicariance is involved, Nothofagaceae being the southern representatives of Fagales that then were distributed world-wide. Further complicating the issue, there are also questionable reports of Caenozoic Nothofagus pollen from the Gulf Coast of the USA as well as in the Pacific North West (Elsik 1974). Or has dispersal shaped the distribution of the family (e.g. Swenson et al. 2001; in particular Sauquet et al. 2011)? Thus Knapp et al. (2005) and Cook and Crisp (2005) suggested that Nothofagus reached New Zealand, at least, by long distance dispersal only ca 30 m.y.a., and Brassospora-type plants have since become extinct there (see also Pole 2003; Waters & Craw 2006; Wallis & Trewick 2009). Kooyman et al. (2014) noted that the Neogene recolonization of New Zealand resulted in rainforests different from those in Australia, etc.. However, Y. Sun et al. (2014) argued strongly for the continued presence of an emergent New Zealand landmass; their focus group was the liverwort Schistochilaceae, common in Nothofagus forests.
Three pollen types occur in the same locality in the Oligocene in Tasmania and the fourth was found nearby (Hill 2001 and references). Since the distribution of Nothofagus currently spans latitudes from almost 0-50+o S, and individual groups have latitudinal preferences, either the climatic preferences of the clades have changed, or there was a very distinctive climate in Tasmania in the Oligocene, or... (Hill & Brodribb 2006). Perhaps this is a late example of the general intermingling of taxa with now very different climatic preferences like that which occurred earlier in the equable early Caenozoic (Palaeocene-Eocene) climates. Similarly, Nothofagus in Miocene Patagonian South America was represented by three pollen types (Palazzesi & Barreda 2007), and all four subgenera are known from Antarctica in the later Cretaceous (see above).
For characters and clades in Nothofagus s.l., see Heenan and Smissen (2013).
Ecology & Physiology. Nothofagaceae have played a major role in more temperate southern hemisphere forests from the later Cretaceous onwards. The late Cenomanian/Early Turonian (ca 93.5 m.y.a.) southermost pollen province is characterized by Nothofagites pollen, probably from plants that would be included in Fagales (e.g. Kedves 1989; Friis et al. 2011). Nothofagoxylon came to dominate angiosperm wood in Antarctica by the mid-Campanian ca 78 m.y.a., and in the Palaeocene and Eocene it further increased in proportional abundance, although conifers may have been replacing non-Nothofagus angiosperms and Nothofagus may not have been very common in Patagonia then (Cantrill & Poole 2005). As Cantrill and Poole (2005, see also 2012) emphasized, different groups of Nothofagus were involved over time - first section Nothofagus predominated, then sect. Lophozonia, while sect. Fuscospora also became quite common in the Eocene and later (see also Kooyman et al. 2014). The ancestral niche for the genus may be mesothermal - or rather cooler, depending on how niches are reconstructed (Hinojosa et al. As the climate in Antarctica deteriorated, N. fusca-type plants in particular persisted until the Pliocene ca 3 m.y.a. if only in tundra-type vegetation, although exactly when woody vegetation finally became extinct is unclear (Cantrill & Poole 2012 for detailed discussion).
Plant-Animal Interactions. The moth Heterobathmia (Heterobathmiidae), jawed moths around 125 m.y.o., is perhaps sister to Agathiphagidae (food plant Agathis), the two diverging perhaps ca 158.5 m.y.a. (Wahlberg et al. 2013; see also Heikkilä et al. 2015), although the latter are more probably one clade down the lep tree and sister to Micropterigidae (Regier et al. 2015; Kristiansen et al. 2015). Heterobathmia makes its home exclusively on Nothofagus, both as an adult - it eats pollen - and as a caterpillar - it is a leaf miner (see also Futuyma & Mitter 1996).
Bacterial/Fungal Associations. Humphries et al. (1986: c.f. more recent ideas of relationships) discuss the parasites and associates of Nothofagus, and suggest the possibility of some co-evolution of the genus with Eriococcus scale insects that grow on it. The inaperturate discomycete Cyttaria grows on Nothofagus in both the Antipodes and South America, but neither in New Guinea nor in New Caledonia. Only subgenera Fuscospora and Lophozonia are affected, and the pattern of association of host and parasite is not simple; the split between Australian and New Zealand species of Cyttaria is estimated at ca 44.6-28.5 m.y. (K. Peterson et al. 2010), overlapping with Crisp and Cook's estimates above.
Tedersoo et al. (2008) examined ECM fungi on Tasmanian Nothofagus), and Tuberaceae and associated clades (ascomycetes) are also found on the genus (Bonito et al. 2013). ECM fungi found on Nothofagaceae and Myrtaceae, both southern groups, are associated, perhaps because the fungi moved from the former onto the latter as the climate became drier (Tedersoo et al. 2008, 2014a).
The rust parasites of Nothofagaceae are rather different from those of other Fagales (Savile 1979).
Chemistry, Morphology, etc. Nothofagus obliqua may have unilacunar nodes; does it have stipules?
Unlike Fagaceae, there is no obvious relationship between the number of fruits and the number of valves of the cupule. The central flower of the cupule often has two carpels, lateral flowers have three. Staminate flowers that apparently have many stamens are interpreted as being the result of the fusion of separate flowers of a dichasium (see also Betulaceae). Embryology is poorly known.
Further information (sometimes under Fagaceae) may be found in Hill and Jordan (1993) and Kubitzki (1993b), both general, Hegnauer (1989: chemistry), Lersten and Horner (2008b: leaf crystals, etc., Fagaceae are similar), Philipson and Philipson (1979: leaf vernation), Rozefelds (1998) and Rozefelds and Drinnan (1998: stamens and staminate flowers), Praglowski (1982: pollen) and Poole (1952: seed). There is also a website, Nothofagus, les hêtres du bout du monde..., nothofagus.free.fr, that will be of interest to francophone visitors.
Phylogeny. Manos (1997), Knapp et al. (2005 and references) and Heenan and Smissen (2013) discuss relationships within the genus; see also Xiang et al. (2014).
Classification. For sections, see Philipson and Philipson (1988), for a checklist and bibliography, see Govaerts and Frodin (1998: in Fagaceae), and for generic limits, see Heenan and Smissen (2013) and Hill et al. (2015).
Previous Pelationships. Nothofagus has often been included in Fagaceae, as by Cronquist (1981) and Kubitzki (1993b).
[Fagaceae [[Myricaceae + Juglandaceae] [Casuarinaceae [Ticodendraceae + Betulaceae]]]: bud scales spiral; leaves spiral; anthers dorsifixed.
Age. Estimates of the age of this node are (65-)61(-57) m.y.a. (Wikström et al. (2001), 62.7 m.y. (Tank et al. 2015: Table S1, S2), and (93-)90, 88(-84) m.y. old (H. Wang et al. 2009: Bayesian relaxed clock estimates up to 100 m.y.). Magallón and Castillo (2009) estimated an age of ca 93.5 m.y., Bell et al. (2010) ages of (68-)55, 55(-40) m.y., and Xiang et al. (2014) an age of (101.2-)99.3(-95.5) m.y. ago. Naumann et al. (2013) offered an age of ca 52.8 m.y. but the age of around 110.3 m.y. in Sauquet et al. (2011) is almost double this.
Evolution. Plant-Animal Interactions. Some larvae of Eriocranidae, a small group of near-basal lepidoptera, are found as leaf miners on this clade (Powell et al. 1998).
FAGACEAE Dumortier, nom. cons. Back to Fagales
Hairs often stellate/branched; sclereid nests in bark, cells with large rhomboidal crystals; veins often associated with crystals only; lamina vernation conduplicate-plicate; inflorescence branched or not; flowers often trimerous; P biseriate [thus = T] or not, 4-6 (7)-lobed; staminate flowers: bract; A (4-)12(-20) (connective produced); pollen not spiny, tectum with ± flat-lying and fused rod-like elements [(micro)rugulate]; pistillode +; carpellate flowers: G , alternating with P, or median member abaxial; ovules bitegmic (unitegmic), supra-chalazal tissue massive, with central strand; embryo sac with chalazal caecum; cupule +, with valves [one more than fruit number], ± spiny; nut trigonous, wall with lignified tissue on the outside, endocarp hairy inside; seeds pachychalazal; (endosperm cellular), 0; germination epigeal; n = 12 (13, 21).
7[list]/670 - 2 subfamilies below. More or less worldwide (map: from Soepadmo 1972; Fl. N. Am. III. 1997).
Age. Estimates for the crown age of the family are 37-34 m.y.a. (Wikström et al. 2001), 77-67 m.y. (Cook & Crisp 2005), (45-)31, 28(-16) m.y.a. (Bell et al. 2010), or around 84.7 m.y. (Sauquet et al. 2012).
The oldest Fagaceae fossils are some 90 m.y. old (Crepet et al. 2004 for references).
1. Fagoideae K. Koch
Plant deciduous; ellagic acid 0; stomata also cyclocytic; leaves two-ranked; staminate flowers: male inflorescence capitate; pollen subprolate-spheroidal, exine fine scabrate; pistillode 0; carpellate flowers: staminodes 0; styles long, recurved, stigma capitate; ovule ?straight, micropyle bistomal, elongate, inner integument thinner than outer, parietal tissue 5< layers across, ?nucellar cap ca 13 cells across; pollen tube at ovule at dormancy; nuts 2/cupule; cotyledons folded; genome size [1C] 0.56-0.63 pg.
1/10. Temperate N. hemisphere. [Photo - Fruiting Branch, © M. Brand.]
Age. An estimate of the crown-group age of Fagoideae is (24.2-)17.2(-7.9) m.y. (Xiang et al. 2014)).
2. Quercoideae Õrsted
(Plant deciduous); (leaves two ranked; whorled), (margins entire; lobed; biserrate); inflorescence spike or catkin, staminate and carpellate flowers on separate inflorescences or not; staminate flowers: sessile; pollen prolate, exine also (micro)verrucate or smooth; pistillode +, (secreting nectar); carpellate flowers: staminodes +; (style relatively long, occupying most of the gynoecium), stigmas capitate, decurrent, or punctiform and with a terminal pore; ovule with integuments the same length [micropyle endostomal?], parietal tissue one cell across, nucellar cap ca 2 cells across, (tracheids +); pollen tubes branched, in style at dormancy; cupule also cup-shaped, with scales; nuts 1-3(-15< - Trigonobalanus)/cupule, (rounded), (endocarp glabrous inside - some subgenus Quercus); (endosperm with basi-lateral caecum); (germination hypogeal); genome size [1C] 0.5-1.3 pg; rpl22 gene transferred from chloroplast to nucleus.
6/640: Quercus (400), Lithocarpus (120), Castanopsis (110). N. temperate, at higher elevations in the tropics, not S. Africa or New Zealand, barely in Australia. [Photo - Fruit]
Age. Estimates of the crown-group age of Quercoideae are around 55.2 m.y. (Sauquet et al. 2012) or (66.1-)56.4(-50.6) m.y. (Xiang et al. 2014).
Synonymy: Castaneaceae Brenner, Quercaceae Martinov
Evolution: Divergence & Distribution. The diversity of the family in the earlier Caenozoic was considerable (Manchester & Crane 1983: fruits very small, ?wind dispersed; Mindell et al. 2007; Kvacek 2008; Denk et al. 2012; Bouchal et al. 2014; Grímsson et al. 2015a: Eocene of W. Greenland). The later Cretaceous Protofagacea, with 6 tepals and 12 stamens, has fruits with a hairy inner wall (Herendeen et al. 1995). For Cretaceous fossil leaves perhaps to be assigned to Fagaceae, see Gnilovskaja and Golovneva (2016).
Extant Fagaceae are often very common in north temperate areas and also on hills and mountains in Central America and Malesia. For character evolution and the biogeography of Fagaceae, see e.g. Manos and Stanford (2001) and Manos et al. (2002). Axelrod (1983; see also Bouchal et al. 2014) discussed the evolution and distributional history of Quercus; the genus is made up of an Old World and a New World clade, with divergence between the two beginning in the Eocene (Hubert et al. 2014). By the end of the Eocene Fagaceae with sclerophyllous foliage evolved in western North American, where conditions were more or less seasonal, and they grew in vegetation similar to modern chaparral and nemoral forest; ecologically similar Fagaceae evolved somewhat later and independently in Europe, and there Mediterranean conditions developed only in the Pleistocene (Bouchal et al. 2014).
For increases in diversification rates in the family see Larson-Johnson (2015: Fig. 10). Bouchenak-Khelladi et al. (2015) discuss the increase of diversification rates within Quercoideae and possible factors triggering this, including moving into Mediterranean-type climates.
Oh and Manos (2006, 2008) suggested that the apparently unitary scaly or spiny cup-shaped cupule that encloses a single, rounded fruit, the acorn, has evolved more than once within Quercoideae, while Cannon and Manos (2001) looked at the evolution of the fruits of a few species of Malesian Lithocarpus in which the cupule almost entirely surrounds the fruit and the smooth, shiny wall of an ordinary acorn is very reduced; the fossil Cascadeicarpa has a similar "doubly inferior ovary" (Mindell et al. 2007: G ).
Ecology & Physiology. Fagaceae frequently dominate the vegetation in which they grow, and their effect on the community is increased by the sometimes rather sporadic episodes of heavy fruiting that are more or less synchronized over quite wide areas, mast fruiting (see below). White oak (Quercus alba) alone represents (12-)19-26(-49)% of witness trees, i.e. trees that were probably present before Europeans arrived, in the oak-dominated forests of eastern North America (81% in some southern Illinois forests). In such forests, (36-)50-80(-± 100)% of all trees are white oak, along with with up to three more ectomycorrhizal (ECM) species, two of which are usually other Fagaceae (Abrams 2003; see also Faison & Foster 2014). Six of the 30 species of Quercus growing in these forests are notable dominants (Abrams 1996). Many oaks like high light and moderately dry conditions, and fires are quite common; oak can replace pine in such situations (Adams 1992). Fagaceae, again mostly Quercus, are abundant in western North America, and in California the black oak, Quercus kelloggii, is particularly widespread and has the greatest timber volume of any oak (Waddell & Barrett 2005). The greatest diversity of Quercus in the New World is in southern Mexico, and Rodríguez-Correa et al. (2015) studied niche divergence in species there and in Central America, suggesting that it was affected by various barriers to dispersal. Species of Quercus subg. Cyclobalanopsis in particular are common dominants of drier sites in tropical lower montane forests in East Asia, in East Malesia in particular, but also in warm temperate conditions (Ashton 2014), while taxa like Castanopsis acuminatissma are conspicuous on the island of Papua.
The ECM American chestnut, Castanea dentata, previously a dominant large tree in some forests in eastern North America and an important source of food for humans and other animals, now persists largely as suckers after its devastation by chestnut blight in the first half of last century (Thompson 2012: dominant over 800,000 km2), however, Faison and Foster (2014) qualify literature reports, i.a. noting that some of the dominance of chestnut was quite recent, being accentuated by coppicing after being cut down by early Europeans. In any event, much of the chestnut forest has since been replaced by mixed oak or oak-hickory forests (Abrams 1996; see e.g. van der Gevel et al. 2012 for the future), so the forests remain dominated by ECM trees.
Fagus-dominated forest may have very little in the way of understory vegetation; Denk and Grimm (2009b) discuss the biogeographic history of the genus.
In holm oak, Quercus ilex, the adaxial surface of the leaf is wettable and can absorb water, the lower side is densely covered in trichomes and is not wettable, so preserving stomatal functioning in wet conditions (Fernández et al. 2014) - see also Bromeliaceae.
Pollination Biology & Seed Dispersal. Quercoideae such as Castanea and Castanopsis are insect pollinated, otherwise, wind pollination dominates in the family. Fertilization is porogamous, according to Johri et al. (1992), although it can be much delayed (Sogo & Tobe 2006d and references; Deng et al. 2008).
Fruits of red oaks (section Lobatae) take one and a half years to mature, overwintering as very small embryos (Stairs 1964 and references) and the seeds are high in tannins and lipids; the fruits of white oaks (section Quercus) mature in about six months and their seeds are less rich in tannins and lipids, furthermore, their seeds tend to germinate faster. Much has been written about the behavior of animals that currently eat and disperse the acorns of these species. Thus squirrels tend to eat the embryos of white oaks before caching the fruits; in general they prefer to eat acorns of white oaks in the fall and to cache those of red oaks (Wood 2005 for literature). For fruit dispersal and habitat preferences, see Xiang et al. (2014: Fagus with winged fruits; c.f. Larson-Johnson 2015).
Some Fagaceae simultaneously, if somewhat erratically, produce large numbers of fruits over large areas, the phenomenon of masting; for accounts of this synchronized but intermittent fruiting, see Koenig and Knops (2000, 2005). The effect of masting on the animals that eat these fruits is considerable (Koening & Knops 2005). As with the mast-fruiting dipterocarps, some of the seed predators like passenger pigeons (Ectopistes migratorius) in eastern North America and wild pigs in Europe are (or were) migratory. The demise of the passenger pigeon, which once made up 25-40% of the total avian biomass in North America, may have been hastened in part by the destruction of its food sources as settlers cleared woodlands for agriculture. Fagaceae - oaks, beech, chestnuts - were a major element in its diet (Curran & Leighton 2000 and references).
Plant-Animal Interactions. Oaks support the highest diversity of herbivores of all temperate holarctic forest trees. Pearse and Hipp (2012) found that leaf defences in Quercus were highest at lower latitudes (little temperature fluctuation, mild winters, low minimum precipitation).
Theclines (Lycaenini) caterpillars are common on Fagaceae (Ehrlich & Raven 1964), while leaf-mining larvae of Eriocraniidae, probably the subbasal clade in the lepidopteran Angiospermivora, eat Fagaceae and Betulaceae (Regier et al. 2015 and references).
By some estimates half of all galls in the north temperate region are found on Fagaceae, especially on oaks - and perhaps especially in North America, where Quercus is particularly diverse (Mani 1964; Abrahamson et al. 1998). Gall wasps (Cynipini) are very nearly all to be found on oaks, and their galls have different morphologies depending on whether they are produced by sexual or agamic individuals; the overall morphological diversity of oak galls is remarkable (Redfern 2011). The some 1,000 species of gall wasps are perhaps two thirds of the known species in the whole Cynipidae (Csóka et al. 2005; Stone et al. 2009). Host plant conservatism here has persisted over the last ca 20 m.y. at least, and major clades of gall wasps usually have associations with major clades of oaks (Stone et al. 2009).
Bacterial/Fungal Associations. Chestnut Castanea dentata forests were utterly devastated by the introduced ascomycete fungus Cryphonectria parasitica (Endothia parasitica) over a period of less than forty years, 1900-1940 (Thompson 2012). Although chestnut plants can persist in the understory for many years after initial infection because they sucker from collars of the dead old trees or from stumps, the suckers practically never reach reproductive age before being reinfected by the fungus (Schlarbaum et al. 1997).
Sudden oak death, caused by the oomycete Phytophthora ramorum has beome a major pathogen on Fagaceae in coastal California and in Oregon over the last 20 years or so, and the infestation is out of control (Cunnliffe et al. 2016)..
Kühdorf et al. (2015: p. 110) noted that the arbutoid "C[omarostaphylis] arbutoides is a refuge plant for ectomycorrhizal fungi as it shares these fungi with ectomycorrhizal tropical trees such as Quercus costaricensis".
Genes & Genomes. For genome sizes in the family, see Chen et al. (2014). Although it was suggested that tropical species generally had larger genomes than temperate species, the smallest genomes were found in temperate species (Fagus, some species of Quercus: Chen et al. 2014).
A mitochondrial gene has moved from the parasite Mitrastemon (Ericales) to its host, Quercus (Systma et al. 2009).
Chemistry, Morphology, etc. Syllepsis is very uncommon in the family (Keller 1994).
There has been much discussion over the morphological nature of the small protrusions surrounding the ovary, and the whole complex is often interpreted as a modified cymose inflorescence (e.g. Sims et al. 1998; Manos et al. 2001a; Pigg et al. 2001; Oh & Manos 2008 for references). When the cupule has valves, probably the plesiomorphic condition, there is one valve more than the number of fruits; the valves represent modified cymose part inflorescences (Fey & Endress 1983).
Endress (1979a) suggested that the flowers of Fagaceae were hexamerous. Denk and Grimm (2009a) describe pollen morphology, focusing on Quercus; I use their terms above (see also Praglowski 1982, 1984); Denk and Tekleva (2014) think about foot layer variation in the family. For the orientation of the carpels, see Endress (1977a) who show the median member of outer T whorl in both staminate and carpellate flowers as being abaxial (c.f. Sims et al. 1998). Variation in ovule and fruit is extensive, and is conveniently tabulated by Deng et al. (2008); the polarity of some of this variation is unclear. Hjelmqvist (1953) discussed the basi-lateral embryo sac/endosperm caecum he noted in some Quercoideae. For intergeneric and intersubfamilial graft hybrids, see Herrmann (1951).
See also Nixon (1989) and Kubitzki (1993b), general, Hegnauer (1966, 1989: chemistry), Loreto et al. (2009: monoterpenes, isoprenoids in Quercus), Huang et al. (2011: ellagitannins with triterpene alcohol cores), Clowes (1951: anatomy of mycorrhizae), Lersten and Horner (2008b: leaf crystals, etc.), Liu et al. (2009: stomata, hairs), and Langdon (1939: ovules, etc.) for additional information.
Phylogeny. Fagus is sister to all other Fagaceae (Manos et al. 1993; Sauquet et al. 2012); Quercoideae s. str. are paraphyletic, Trigonobalanus being sister to the rest of the clade. For phylogeny see also Manos and Stanford (2001), Manos et al. (2002) and Xiang et al. (2014); support for the position of Trigonobalanus was not that strong and Quercus was paraphyletic - or at least its monophyly was unclear - in the latter study. Li (1996) did not find Fagaceae to be monophyletic in his morphological analysis.
Trigonobalanus was long known from Fraser's Hill in Peninsula Malaya, but was first described only some 55 years ago from Mt Kinabalu in Borneo, it was then found in South America 35 years ago, and then fossil in North America... The three extant species have been placed in three genera, but they form a single clade (Nixon & Crepet 1989 for information).
Oh and Manos (2006, 2008) suggest that Lithocarpus, which has fruits like those of Quercus, is polyphyletic, the South East Asian members grouping with Chrysolepis. Indeed, the single species from the Californian floristic province of West North America, L. densiflorus (now = Notholithocarpus), is in a clade with Quercus, Castanopsis, and Castanea. Quercus contains both species with fast-maturing (a few months) acorns and a pericarp that is glabrous inside - both derived characters - and species in which the acorns take 1 1/2 years to develop and the endocarp is hairy inside. For phylogenetic relationships within Quercus, see Manos et al. (1999), Oh and Manos (2008) and especially Hubert et al. (2014). However, detailed relationships may be difficult to disentangle if the various positions that different accessions of species like Q. ilex, Q. suber and Q. robur appear on the one tree is any indication (Simeone et al. 2013); relationships were also affected by the outgroup chosen (Hubert et al. 2014). For relationships in North American oaks, see Manos et al. (1999), Pearse and Hipp (2009) and Hipp et al. (2014), and for relationships in Quercus subgenus Cyclobalanopsis, poorly resolved, see Deng et al. (2013).
Classification. Govaerts and Frodin (1998) provide a checklist and bibliography for the family.
[[Myricaceae + Juglandaceae] [Casuarinaceae [Ticodendraceae + Betulaceae]]] / the Normapolles group: myricetin +; pollen tripororate, exine of two layers separated by an alveolar zone and obviously expanded around the apertures, exine infratectum granular, intine thickening at the apertures [= oncus] [?level]; G ; fertilization chalazogamous.
Age. This node has been dated to 47-46 m.y. (Wikström et al. 2001), (50-)41, 37(-28) m.y. (Bell et al. 2010), or as early as (96.9-)93.4(-88.2) m.y. (Xiang et al. 2014, but c.f. topology).
Evolution: Divergence & Distribution. Lithocarpus, basically South East Asian-Malesian, is widespread as fossils in the northern hemisphere and there are recent preliminary reports of it in Early Eocene deposits from Patagonian Argentina (M.-Q. Liu & Zhou 2006; Hermsen & Gandolfo 2016).
The pollen of Betulaceae and Juglandaceae in particular is rather like that of the fossil Normapolles type, and they all have a granular exine infratectum (e.g. Doyle 2009); see Christopher (1979) and Batten (1980) for the classification of these grains, also papers in Rev. Palaeobot. Palynol. 35(2-3). 1981. Batten (1989; see also Clarke et al. 2011) was cautious about the organismal connections of these grains, not all of which may have come from members of Fagales, and the grains did not always seem to him to be of wind-pollinated plants (Batten 1981). As he observed, "In due course it may be reasonable to refine the Normapolles as a distinct pre-juglandalean/myricalean order for plants which produced pollen grains of the Trudipollis-Oculipollis type and morphologically comparable forms" (Batten 1989: p. 19), and he even thought that Betulaceae, for instance, might not have Normapolles-producing ancestors. Further confusing the issue, Larson-Johnson (2015) placed a number of fossils purportedly of Normapolles-producing plants outside crown-group Fagales. Odd character combinations in pollen of late Campanian/early Maastrichtian age ca 70.6 m.y.a. have even been explained as the result of hybridization (Hofmann et al. 2011). Normapolles-type grains have also been compared with those of Urticaceae and relatives and Proteaceae (Batten 1981), while Feuer (1991) did not find much similarity between the pollen of many extant members of this clade.
There is much variation in Normapolles-producing fossil flowers (see Friis et al. 2006a, especially 2011: e.g. chap. 14.6.6, Fig. 20.6, etc.). The flowers are usually perfect and with a simple, undifferentiated perianth. In Bedellia staminate flowers only are known, and these have two five-parted perianth whorls; Caryanthus has a four-parted perianth with six stamens in two groups of three (Sims et al. 1999: Table 2). Normanthus, from the late Cretaceous of Portugal, has five quincuncial perianth members that alternate with the stamens, and there are two collateral carpels with separate and quite long styles; the placentation is described as being parietal, with one ovule/carpel (Schönenberger et al. 2001b). Endressianthus has imperfect flowers, with four stamens alternating with the perianth members in the staminate flowers (Friis et al. 2003a), while Dahlgrenianthus has five stamens opposite the perianth members and a superior ovary with short, more or less separate styles (Friis et al. 2006a). As with other fossil Fagales (see above), relating these fossils to extant families is a challenge.
That being said, Normapolles pollen was abundant in the Turonian-Campanian of the Cretaceous, some 94-80 m.y.a., peaking in the Coniacian-Santonian ca 88 m.y.a., and occurring in much of the Northern Hemisphere from west Siberia to east North America in particular in the area 20-45oN (Cretaceous palaeolatitude: Kedves & Diniz 1983; Kedves 1989; Sims et al. 1999; Friis et al. 2003a, esp. 2006a, 2011: Figs 20.6, 7 for summaries); Aquilapollenites, variously linked with Santalales (e.g. Jarzen 1977), Apiaceae, and Caprifoliaceae-Morinoideae, is found in between this area and it is also circumboreal (Vakhrameev 1991; Farabee 1993). Trees that perhaps produced Normapolles pollen may have dominated open late Cretaceous (Campanian) woodland in Texas (Lehman & Wheeler 2001), but this needs confirmation.
Details of wood anatomy, including the presence of chambered crystals in the axial parenchyma, that are common in this group (Carlquist 2002c) may properly be features of Fagales as a whole.
Ecology & Physiology. Taxa that have cluster roots, usually associated with an enhanced ability to take up phosphorus, and are also able to fix nitrogen are scattered through this clade (Myricaceae, Casuarinaceae, Betulaceae: Lambers et al. 2008).
Chemistry, Morphology, etc. Normapolles pollen is oblate in shape and triaperturate with protruding, elaborate and strongly thickened apertural regions, the apertures themselves often being formed from expansions of the granular infratectal layer (see also Feuer 1991); the result is that the pollen is more or less triangular in transverse section. The apertures have internal pores and externally short colpi or pores. The wall is usually tectate-granular, but there is sometimes an atectate polar zone, the surface being almost smooth to finely spinulate to rugulate. The infratectum is granular (details from Friis et al. 2003a).
[Myricaceae + Juglandaceae]: chains of crystal-containing cells in the wood; sieve tube P-protein bodies 0; peltate glandular hairs +; stipules 0; 1 flower/bract; stigma lamellular/laciniate; ovule single [per flower], straight, erect; x = 8, longest chromosome with (sub)median secondary constriction.
Age. This node has been dated to ca 47.1 m.y. by Tank et al. (2015: Table S2), 38-36 m.y.a. (Wikström et al. 2001) or (43-)32, 29(-11) m.y. (Bell et al. 2010), but see other dates below.
The age of a node [Myricaceae + The Rest] is estimated at (94.6-)90.4(-85.0) m.y. (Xiang et al. 2014, see topology).
Evolution: Divergence & Distribution. The evolution of features of inflorescence and ovule is particularly difficult to understand; they could be synapomorphies of the clade as a whole (as above), or be independent apomorphies of Myricaceae and Juglandaceae-Juglandoideae. Herbert et al. (2006) discuss possible synapomorphies around here.
Chemistry, Morphology, etc. The leaf teeth in Myricaceae in particular, see also Cuinoniaceae, etc., are intermediate in "type" and venation characters do not distinguish sharply between Cunoniaceae and Fagales (see Hickey & Taylor 1991).
MYRICACEAE Kunth, nom. cons. Back to Fagales
Lamina vernation conduplicate to curved; plants dioecious or monoecious; staminate flowers: A (opposite P); carpellate flowers: G [(3)], ?superior to inferior; ovule basal; fruit a drupe; seed ?pachychalazal, testa ± thickened; endosperm slight or 0; n = 8, 12.
4[list]/57: two groups below. ± Cosmopolitan, scattered (map: Hultén 1958; van Balgooy 1974; Trop. Afr. Fl. Pl. Ecol. Distr. 5. 2010).
Age. An age of (81.7-)69.7(-60.4) m.y. for crown-group Myricaceae is suggested by Xiang et al. (2014).
Fossil pollen attributed to the family is Cretaceous-Cenomanian (97.5-91 m.y.a.) in age (H.-L. Li et al. 2015).
1. Canacomyrica Guillaumin
?Nodes; P connate, 6-lobed; staminate flowers: A 6; pistillode +; carpellate flowers: staminodes +; ovule ?bitegmic, micropyle much elongated; ?fertilization; in fruit micropyle becoming still more elongated, recurved.
1/1: Canacomyrica monticola. New Caledonia (map: above, green).
Synonymy: Canacomyricaceae Doweld
2. The Rest.
(Plant deciduous); roots with N-fixing Frankia nodules, rootlets clustered, of limited growth [Proteoid roots]; nodes also 1:1; (lamina pinnatifid), (stipules ?foliaceous, lobed Comptonia); P 0; staminate flowers: A 2-8(-20); carpellate flowers: staminodes 0; integument 3-7 cells across, parietal tissue 6-9 cells across, nucellus apex exposed, central nucellar strand of elongated cells; megaspore mother cell single; fertilization porogamous.
3/55: Morella (46). ± Cosmopolitan but scattered, not in the southern half of South America nor south and east of New Guinea (map: above, red). [Photos - Collection.]
Age. The crown-group age of this clade is estimated at around 24.9 m.y.a. (Sauquet et al. 2012), (58.6-)54.3(-49.6) m.y. (Xiang et al. 2014), or (95.7-)71, 69.8(-55.1) m.y. (H.-L. Li et al. 2015).
Evolution: Divergence & Distribution. Comptonia, now restricted to eastern North America, was widespread in the Northern Hemisphere (including Greenland) in the Caenozoic, with some records dating from the Late Cretaceous; most of the records are of the distinctive foliage (Liang et al. 2010). Canacomyrica, now endemic to New Caledonia, has been reported from New Zealand as recently as 17-11 m.y.a. (D. E. Lee et al. 2001).
Ecology & Physiology. Myricaceae - but not Canacomyrica - are associated with nitrogen-fixing Frankia and cluster roots are also developed; mycorrhizae appear to be absent (Hurd & Schwintzer 1997). Carboxylate exudation may help in phosphorus acquisition (Lambers et al. 2012b).
Pollination Biology & Seed Dispersal. Although fertilization is porogamous, it is delayed as in other Fagales, the pollen tubes pausing in their growth on the nucellar surface, which is at least initially exposed; this method of fertilization, described as pseudoporogamy, is derived (Sogo & Tobe 2006a, b: perhaps two characters - no micropyle, but pollen tube enters the ovule at the "micropylar" end). The flowers of plants of some species differ in sex from year to year (Jurzyk 2005 and references).
Bacterial/Fungal Associations. Both AM and/or ECM associations have been reported from Myricaceae (e.g. Rose 1980).
Chemistry, Morphology, etc. Hickey and Taylor (1991) showed a leaf of Canacomyrica in which two adjacent teeth were cunonioid and rosid respectively.
Bracteoles may be present or not. Although the ovary appears to be superior, as in Comptonia, it is often so highly reduced that any traces of its inferior construction would be lost, however, in Canacomyrica, from New Caledonia, staminodes are borne on top of the ovary and there is a six-lobed perianth. In some species of Myrica the ovary is invested by tissue from a meristem developing below the flower, even below the bracteoles, which are then borne on the flower. The flowers of Canacomyrica have three "bracts" (Herbert et al. 2006) - do these represent a floral bract plus two bracteoles/prophylls? Kubitzki (1993b) draws the ovule of Canacomyrica as being basal, straight, and with a much elongated integument forming an apical tube (see also Macdonald 1989); Herbert et al. (2006) simply describe the ovules as being bitegmic.
For chemistry, see Hegnauer (1969, 1990), for floral morphology, very tricky to interpret, see Macdonald (1978, 1979 and references) and Leroy (1957: Canacomyrica), for general information, see Kubitzki (1993b), and for wood anatomy, see Carlquist (2002c).
Phylogeny. Relationships within Myricaceae are likely to be [Canacomyrica [Comptonia + The Rest]] (Herbert et al. 2006; Xiang et al. 2014: support strong; M. Sun et al. 2016), which, depending on the phylogeny of the order, could have interesting implications for character evolution. Huguet et al. (2004) found the relationhips [Myrica + Comptonia] other Myrica], the two clades being colonized by different strains of Frankia.
Classification. If the topology of Huguet et al. (2005) holds, then the limits of Myrica will have to expanded or contracted.
JUGLANDACEAE Perleb, nom. cons. Back to Fagales
Xylem with gelatinous fibres; buds lacking scales; leaves compound, odd-pinnate; P 4; pollen scabrate; carpels median, apically 1-locular, stigmas decurrent, ± recurved; endosperm 0.
9[list]/51, three groups below. North temperate, also Malesia and the Andes.
Age. Crown-group Juglandaceae are estimated to be around 85.8 m.y. (Sauquet et al. 2012) or (96.4-)79.9-(71.2) m.y.o. (Xiang et al. 2014).
1. Rhoipteleoideae Reveal
Plant deciduous; chemistry?; cork?; sieve tube protein bodies?; leaves two-ranked, leaflets alternate, stipules +, asymmetrically caudate; inflorescence branched-catkinate; flowers in triads, central flower perfect; A 6; pollen 3-colporate, ectoapertures elliptic, not round, exine folded [plicate], vestibulum 0, endexine lamellate, thick at the apertures; G, adaxial fertile, stigmas commissural, flattened; ovule campylotropous, bitegmic, micropyle?; ?fertilization; fruit a samaroid nut; P persistent; testa?; ?seedling; n = 8.
1/1: Rhoiptelea chiliantha. China, northern Vietnam (map: from Fu 1992).
Synonymy: Rhoipteleaceae Handel-Mazzetti, nom. cons.
[Engelhardtioideae + Juglandoideae]: flavones, naphthoquinones, raffinose and stachyose [phloem exudate] +; xylem with banded parenchyma; nodes also 5:5; leaves spiral, leaflets subopposite, (margins entire); (inflorescence branched); (P 0-3); staminate flowers: A 4-many; pollen 2-20 porate, apertures usu. elongate, endexine homogeneous, not at the apertures; pistillode +; carpellate flowers: ?staminodes; [(G 3, 4)], when 3, median member adaxial, loculi ± divided [false septum], (stigmas not decurrent), (commissural); ovule borne at the top of the septum, straight, erect, integument 6-10 cells across, (lobed), parietal tissue 3-11 cells across; megaspore mother cells numerous; (fertilization porogamous); fruit drupaceous, nut, samaroid, or winged by persistent bracts, pericarp intrusive; seeds (large [>1.5 cm long]), pachychalazal; endosperm very slight or 0, cotyledons much folded; genome duplication, x = 16, second longest chromosome with (sub)median secondary constriction.
Ca 8/50. North temperate, S. to Argentina and Malesia. [Photo - Collection.]
Age. The crown group is around 72.6 m.y.o. (Sauquet et al. 2012) or (75.9-)70.6(-64.1) m.y.o. (Xiang et al. 2014).
The oldest fossils that have been placed in Juglandoideae are some 98-83 (Budvaricarpus: see Hermanová et al. 2011) or 88-73 m.y.o. (Crepet et al. 2004 for references) or 78 m.y.o. (Manos et al. 2007: the age of Caryanthus). However, both genera are placed outside crown-group Fagales(!) in the combined molecular-morphological study of Larson-Johnson (2015).
2. Engelhardtioideae Iljinskaya
Plant ?; vessel elements with simple and scalariform perforation plates; leaf parenchyma with druses [basal condition - none]; leaves (opposite), even-pinnate, leaflets usu. entire, (vernation involute or ± conduplicate - Alfaroa); carpellate flowers: inflorescence catkinate; bracts 3-lobed, bracteoles 0-2, ± abaxial, adnate to lower half of ovary; nuts with a layer of fibrous cells in wall.
3-4/14. Himalayas to Malesia, Mexico to Colombia (map: see Meusel et al. 1965; Manchester 1987).
Age. The crown-group age of this clade is around 36.2 m.y. (Sauquet et al. 2012); estimates in Manos et al. (2007) are around 44 m.y. and in Xiang et al. (2014) (49.4-)37.7(-28) m.y. (see also below).
Synonymy: Engelhardtiaceae Reveal & Doweld
3. Juglandoideae Eaton
Plant ?; vessel elements with simple perforation plates alone; (pith chambered); (leaflet vernation involute - Pterocarya); (inflorescence erect and almost cone-like); plant heterodichogamous; staminate flowers: bracts 1-lobed; pollen usu. at least 26 µm across [17-26 µm is the plesiomorphic condition], (4< porate); carpellate flowers: bracts unlobed, bracteoles usually lateral, adnate at least to half the ovary; (G collateral); (nucellar cap ca 2 cells across - Juglans); nuts with sclereids in wall, (endocarp with lacunae), (outer part of fruit splitting - Carya); polyploidy common, (n = 11, 12, 14, 15).
5/35. Temperate N. hemisphere, only 1 sp. in Europe, Central America and down the Andes, but not native in Brazil (Souza & Lorenzi 2012), c.f. versions prior to vii.2014 (map: see Meusel et al. 1965; Manchester 1987).
Age. Crown-group Juglandoideae have been dated to around 65 m.y.a. (Sauquet et al. 2012), while Manos et al. (2007) gave a range of estimates between about 52 to ca 67 m.y.; there is an estimate of (69.7-)66.6(-62.6) m.y. in Xiang et al. (2014). On the other hand, Bell et al. (2010) suggested that Carya and Juglans (on the two main branches of this clade) diverged only (8-)4(-1) m.y.a. and Wikström et al. (2001) suggested an age of 7-6 m. years.
Polyptera manningii, a well-understood fossil common in what is now SW Wyoming as much as 65 m.y.a., is assignable to this subfamily; its pollen is 24-30 µm (Manchester & Dilcher 1997; Donovsn et al. 2016).
Synonymy: Platycaryaceae Doweld
Evolution: Divergence & Distribution. Several extant genera found as fossils in North America and especially Europe do not grow there now (Manchester 1987); for the early Caenozoic fossil history of what are now East Asian endemics, see Manchester et al. (1987, 2009). Thus fossil pollen of Rhoiptelea is known from E. North America (Fu 1992). Friis et al. (2011) note that some fossils are very similar to Rhoiptelea chiliantha, but they have a half-inferior ovary; the ovary of Rhoiptelea is presumably secondarily superior. A number of extinct genera, some showing very interesting combinations of characters, are known from early Caenozoic deposits in North America, and the family was very diverse there (Manchester 1991; Elliott et al. 2006). There are recent reports of Engelhardioideae (as Alatonucula, also pollen records) from the early Eocene of Patagonian Argentina, far south of the current distribution of the subfamily, in deposits at least 47.8 m.y.o. (Hermsen & Gandolfo 2016).
Details of diversification in the family are unclear, and there is great variation in the age estimates for Juglandoideae in particular (Manos et al. 2007). Manos et al. (2007) and particularly Larson-Johnson (2015) integrate the rich fossil record with the phylogeny of the family (see also Manchester 1987). Diversification in the Rhoiptelea clade has decreased (!: Larson-Johnson 2015). Manos and Stone (2001) put morphology in the context of phylogeny.
Ecology & Physiology. Oreomunnea may dominate forests in Panama (references in Peay 2016). Interestingly, it seems that despite strong negative plant-soil feedback at the seedling stage, monodominant stands of Oreomunnea mexicana formed because the ectomyccorhizal fungal associated with the plant could obtain nitrogen directly from organic matter (Corrales et al. 2016).
Pollination Biology & Seed Dispersal. There is a form of heterodichogamy in several [Engelhardoideae + Juglandoideae] (Renner 2001 for references; Fukuhara & Tokumaru 2014). Platycarya (Engelhardioideae) is distinctive in having sticky pollen and strongly scented flowers, which suggests insect, perhaps thrip, pollination (Li et al. 2005 and references; Fukuhara & Tokumaru 2014).
Taxa with biotic dispersal of their seeds may have evolved in the Caenozoic from wind-dispersed taxa (Tiffney 1986a: early Caenozoic; Larson-Johnson 2015: somewhat later).
Genes & Genomes. A duplication of the whole genome can be placed at the [Engelhardoideae + Juglandoideae] node (Luo et al. 2014).
Chemistry, Morphology, etc. Genera with opposite leaves (Alfaroa, Oreomunnea) have spiral leaves in seedlings.
Triads of flowers are found as abnormalities in the [Engelhardoideae + Juglandoideae] clade (Manning 1940) and of course in Rhoiptelea (see above). The fossil Budvaricarpus has similar triade that are surrounded by a common bract (Hermanová et al. 2011). Perfect flowers are known from Platycarya, although normally the cone-like inflorescences have staminate and carpellate flowers together and the bracts are not part of the fruit (Li et al. 2005). For discussion on the nature of the bract/perianth-type structures associated with the flowers, especially the carpellate flowers, see Lin et al. (2016)); in Juglans regia, for example, they show a more or less annular rim encircling the carpellate flower, and a bract develops from this in the axial position and a single bracteole in a (sub)adaxial position - rather odd.
The staminate flowers of Juglans regia and Engelhardia spicata are monosymmetric (Lin et al. 2016). The pollen surface is almost microspinulose (Stone & Broome 1975). The stigma may be commissural or not and the orientation of the carpels varies (Manchester 1987; Manos & Stone 2001 for summaries); thus all three gynoecia of a Budvaricarpus triad are shown as having carpels with the same orientation, although this is supposed to be a cymose unit (Hermanová et al. 2011).
For general information, see Manchester (1987) and Stone (1993), for chemistry, see Hegnauer (1966, 1989), for fertilization, see Luza and Polito (1991 and references), and for karyomorphology, see Oginuma (1999). Rhoiptelea in particular: For chemistry, see Hegnauer (1990), for pollen, see Stone and Broome (1971) and Friis et al. (2006a), for the breeding system, Sun et al. (2006), and for general information, see Wu and Kubitzki (1993).
Phylogeny. For relationships in the family, see Gunter et al. (1994) and especially Manos and Stone (2001); Engelhardia is paraphyletic, and monophyly of Engelhardoideae and Juglandoideae is well supported. Platycarya is often sister to other Juglandoideae, but its position there is not clear (Manos et al. 2007; see also Sauquet et al. 2012; Larson-Johnson 2015). Engelhardia s. str. is sister to the rest of Engelhardoideae (Manos & Stone 2001; Manos et al. 2007).
Classification. Including Rhoipteleaceae in Juglandaceae s.l. was optional in A.P.G. II (2003); the two were merged in A.P.G. III (2009).
Manos and Stone (2001) provide a revised classification of [Engelhardoideae + Juglandoideae], and there have been some subsequent adjustments of generic limits.
[Casuarinaceae [Ticodendraceae + Betulaceae]]: dihydroflavonols +[?]; pollen tubes branched; stigmas elongate.
Age. Distributions of ages of this node are bimodal and non-overlapping - some 40.7 m.y.a. in Tank et al. (2015: Table S2), 36-35 m.y.a. (Wikström et al. 2001) and (36-)29, 27(-18) m.y.a. (Bell et al. 2010), or up to 81-71 m.y. (Cook & Crisp 2005), ca 87.2 m.y. (Sauquet et al. 2012), (88.6-)82.8(-74.7) m.y.a. (Xiang et al. 2014) and (97-)92.5, 90(-84.3) m.y. (H.-L. Li et al. 2015).
The age in Cook and Crisp (2005) was driven in part by the assignment of the fossil Endressianthus, ca 71 m.y.o., to the stem of this clade.
Evolution: Pollination Biology & Seed Dispersal. Sogo and Tobe (2008) suggest that the chalazogamous fertlization that occurs in all families of this clade is similar down to the details of where the pollen tube growth is temporarily delayed. Pollen tubes may branch when they have "lost their way" (Sogo & Tobe 2008: p. 624).
CASUARINACEAE R. Brown, nom. cons. Back to Fagales
Roots with N-fixing Frankia, rootlets clustered, of limited growth [Proteoid roots]; flavonols, biflavonoids +, flavones, myricetin 0; nodes 1:1; banded apotracheal parenchyma +; broad compound rays + (0); stem thin, green, photosynthetic, stomata usu. tetracytic [hidden], transversely oriented; leaves 4-16-whorled, scale-like, margins entire, stipules 0; plant monoecious or dioecious, inflorescences capitate-spicate, one flower/bract, bracts and bracteoles ± well-developed; staminate flowers: P 2 ["inner bracteoles"], median; A 1, filament incurved in bud, anthers ± longer than connective, thecae separate or not; tapetal cells uni(bi-)nucleate; pollen infratectum not granular; pistillode 0; carpellate flowers: bracteoles large; P 0; staminodes 0; G with abaxial member only fertile, stigma wet; ovules bitegmic, micropyle endostomal or nucellus apex exposed, outer integument 3-4 cells across, inner integument 2-3 cells across, parietal tissue 5-8 cells across, supra-chalazal tissue massive, central tracheids +, vascular bundle branched in chalaza; megaspore mother cells numerous, embryo sacs several, chalazal caecum +, (reaching the funicle); fruit a samara, freed as the much accrescent bracteoles separate; seed coat adnate to pericarp; endosperm 0; n = 8[Gymnostoma]-14; germination epigeal, phanerocotylar.
4[list]/95. South East Asia and Malesia to the S.W. Pacific, esp. Australia (map: from Coetzee & Muller 1984; Fl. Austral. 3. 1989; fossils blue, see references below). [Photo - Collection.]
Age. The beginning of divergence within Casuarinaceae has been dated to (65.7-)56.2(-45.3) m.y.a. (Xiang et al. 2014).
Evolution: Divergence & Distribution. Casuarinaceae fossils are known from Caenozoic deposits in South Africa, the Ninety East Ridge in the Indian Ocean, and Argentina (Coetzee & Muller 1984; Hill & Brodribb 2001); material from the Eocene ca 52.2 m.y.a. of Patagonia has been placed in Gymnostoma (Zamaloa et al. 2006). Casuarinaceae were especially prominent in the lower Middle Miocene of New Zealand (Lee et al. 2001; Pole 2003).
The diversification rate increased in Allocasuarina (Bouchenak-Khelladi et al. 2015), and this 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).
Ecology & Physiology. A number of Casuarinaceae are halophytes (Moray et al. 2015). For a switch from scleromorphy (Gymnostoma) to xeromorphy, perhaps some time in the Miocene, see Hill and Brodribb (2001).
Nitrogen-fixing is known from the family, and Casuarina oligodon plays an important role in agriculture in parts of montane New Guinea, both in providing firewood and in fixing nitrogen for the sweet potato crop (Golson & Garner 1990). Cluster roots, probably enhancing phosphorus uptake, are also common; cluster roots, gram-positive N-fixing actinomycetes, and ECM make a very unusual combination (Shane et al. 2006; Lambers et al. 2008).
Bacterial/Fungal Associations. The N-fixing Frankia strains of Casuarinaceae live in a close to obligate association with their hosts, and have not been found in the soil outside the native range of the family (Norman et al. 2006). See Subbarao and Rodríguez-Barranco (1995) for microbes associated with Casuarina. In New Caledonian Gymnostoma, at least, there are root nodules, modified roots, that are formed in association with ECM fungi (Duhoux et al. 2001), however, species like C. glauca may be AM (Duponnois et al. 2003; see also Rose 1980).
Chemistry, Morphology, etc. Do flavananols occur in this family? The starch grains are distinctive (Czaja 1978). Crystals have been observed in the cuticle (Flores & Moseley 1982).
The texture of what some have called the outer and inner bracteoles of the staminate flowers is very different; the latter are called the perianth here, however, inflorescence development is clearly very complex (Flores & Moseley 1982). In a floral diagram, Swamy (1948b) illustrated collateral carpels, but he talked about the carpels as if they were superposed (as also in Swamy 1955). The ovules are described as being orthotropous (straight) by Johnson and Wilson (1993), but they are drawn as anatropous by Treub (1891), Swamy (1948b) and Flores and Moseley (1982). Although Swamy (1944, 1948b) talked about quite well developed parietal tissue in the ovule, in the first article a well-developed nucellar cap is illustrated. The nucellus of Casuarina montana (= C. junghuhniana) protrudes broadly between the integuments, so the apex of the nucellus is exposed and there is a sort of nucellar beak; this is because of the great development of the megaspore mother cells in the lower part of the nucellus (Swamy 1948).
There are no intermediates between the cotyledons and scale leaves, and there is a whorl of buds at the cotyledonary node (Hwang & Conran 2000).
See also Rogers (1982a), Dilcher et al. (1990) and Johnson and Wilson (1993) for general information; also Hegnauer (1964, 1989: chemistry), Poisson (1874: stem anatomy), Moseley (1948: wood anatomy),and Sogo et al. (2001: fertilization).
Phylogeny. Steane et al. (2003) provide a phylogeny of the family. Gymnostoma is sister to the rest (see also Xiang et al. 2014; M. Sun et al. 2016) and it also has many plesiomorphous features. Both its carpels are fertile (although this feature is likely to be an apomorphy, given the situation in the rest of the order), with 2 ovules/carpel, its stem stomata are not hidden, and perhaps n = 8.
Classification. Although the monophyly of Causarina s.l. has never been in doubt, it has been split into four genera, themselves monophyletic.
[Ticodendraceae + Betulaceae]: sclereid nests in bark, cells with large rhomboidal crystals; mucilage cells +; leaves two-ranked; anther thecae ± separate.
Age. The age of this node is about 302-211 m.y. (Forest et al. 2005: huge confidence intervals), around 76.7 m.y. (Sauquet et al. 2012), about 143 or 88 m.y. (Grimm & Renner 2013), or (80.3-)74.0(-66.9) m.y. (Xiang et al. 2014).
TICODENDRACEAE Gómez-Laurito & L. D. Gómez P. Back to Fagales
Buds not perulate?; foliar hypodermal idioblasts +; hairs T-shaped, unicellular, not glandular; lamina margin serrate, stipules encircling the stem; plant (polygamo-)dioecious; staminate flowers: inflorescence erect; P 0; A 8-10+, filaments = or longer than anthers; carpellate flowers: flower single; ?P minute, connate; (staminodes +); G ?tangentially arranged, with divided loculi; ovules hemitropous, integument 20-30 cells across, parietal tissue ca 6 cells across, nucellar cap 0; fruit large, drupaceous, stone longitudinally ridged; exotestal cells initially radially elongated, all cells ± thick-walled and tanniniferous; endosperm development?; n = 13.
1[list]/1: Ticodendron incognitum. Central America (map: from Hammel & Burger 1991). [Photo - Fruit.]
Evolution: Divergence & Distribution. Ferrignocarpus fruits assignable to Ticodendraceae have been found in Eocene deposits from Oregon and in the London Clay; they are up to ca 50 m.y.o. (Manchester & Renner 2005; Manchester 2011). Chambers and Poinar (2014) report female flowers from Tertiary Dominican amber.
Chemistry, Morphology, etc. The nodes are trilacunar, judging from the condition in the outer cortex. Lersten and Horner (2008c) describe hypodermal idioblasts (they also occur below the midrib); these sometimes contain druses, and the authors suggest that they may be an apomorphy for the family. Almost all the leaf teeth are vascularized directly by secondary veins, unlike Betulaceae.
The bracteoles of the carpellate flowers have groups of vascularized scales in their axils, suggesting that the carpellate inflorescence has a fundamentally cymose construction. Interestingly, Feuer (1991) did not find much similarity between the pollen of Ticodendron and that of Juglandaceae, Fagaceae, Nothofagaceae, or even Betulaceae. The embryology is poorly known, but the vascularization of the integument is extremely well developed.
For information, see Kubitzki (1993b: general), Carlquist (1991a: wood), Tobe (1991: floral morphology), and Sogo and Tobe (2008: fertilization).
Classification. For a checklist and bibliography, see Govaerts and Frodin (1998).
BETULACEAE Gray, nom. cons. Back to Fagales
Flavones +; stratified phloem +; sieve tube P-protein usu. 0; lamina vernation usu. laterally or vertically conduplicate, margin doubly serrate, colleters +; plant monoecious or dioecious, catkinate, (bracts peltate); P 0-6, staminate flowers: filaments ± divided), anthers longer than connective; pollen starchy; pistillode 0; carpellate flower: inflorescence catkinate; staminodes 0; G [(3)], collateral, septae incomplete, (short style +); ovules (1-4/carpel), collateral (superposed), lower part of integument vascularized; embryo sacs several; endosperm slight; n = 8, 11, 14; horizontal transfer of rps11 gene; sporophytic incompatibility system present.
6[list]/145 - 2 groups below. North Temperate, to Andes and Sumatra (map: from Meusel et al. 1965; Hultén 1971). [Photo - Flower.]
Age. Crown-group Betulaceae may be around 131-115 m.y. (Forest et al. 2005: large confidence intervals), about 64 m.y. (Sauquet et al. 2012), about 63-43 m.y. (Grimm & Renner 2013: preferred age, one estimate twice this), (72.5-)64.4(-59.4) m.y. (Xiang et al. 2014), or (88.6-)85.9, 83 m.y. (H.-L. Li et al. 2015: Alnus sister to the rest of the family). Crown and stem ages of 25 and 36 m.y.a. respectively were suggested by Quirk et al. (2012).
The oldest fossils possibly assignable to the family are from 94-83 m.y.a. (see Crepet et al. 2004 and Forest et al. 2005 for references); Bedellia pusilla, the plant involved, was described from east North America (Sims et al. 1999; not included in Larson-Johnson 2015). Normanthus and Endressianthus (see above), from the late Cretaceous of Portugal, may also be close to the root of the Betulaceae clade (Friis et al. 2005, see esp. 2011), but the former is described as having perfect flowers with five perianth members alternating with the stamens and an ovary with parietal placentation (Schönenberger et al. 2001b; Friis et al. 2003a). Both are placed outside crown-group Fagales by Larson-Johnson (2015).
1. Betuloideae Arnott
Plant deciduous; spirally-thickened vessel elements 0; peltate glandular hairs +; (prophyll adaxial - Alnus), (buds naked - some Alnus); (leaves spiral - Alnus); staminate flowers: pollen (4< porate), endexine lamellate; carpellate flowers: (inflorescence cone-like - Alnus); P 0 (2); parietal tissue 1-2 cells across, nucellar cap ca 2 cells across; (megaspore mother cell 1); infructescence with woody or scaly bracts separate from fruit, nut small [<3 mm long], ± flattened, samaroid; genome size [1C] 0.2-0.75 pg.
2/95: Betula (60). N. hemisphere, to about 28o S. along the Andes in South America.
Age. The two genera diverged 25-19 m.y.a. (Wikström et al. 2001) or (28-)20, 18(-10) m.y.a. (Bell et al. 2010). Other estimates are older: 109-92 m.y. (Forest et al. 2005: large confidence intervals), about 60-38 m.y. (Grimm & Renner 2013: preferred age, some estimates almost twice this), or (66.0-)59.6(-46.8) m.y. (Xiang et al. 2014: the crown group ages of the two genera are about half this).
The earliest records of the distinctive infructescences of Alnus are Palaeocene in age (X. Liu et al. 2014).
2. Coryloideae J. D. Hooker
Plant usu. deciduous; spirally-thickened vessel elements +, tracheids +; lamina vernation conduplicate-plicate [Corylus]; cymule with <3 flowers; staminate flowers: P 0; A hairy; carpellate flowers: (inflorescence 1-5-flowered, ± erect - Corylus); P +, uniseriate; integument ca 6 cells across, parietal tissue 4-8 cells across, nucellar cap 0-2 cells across, supra-chalazal tissue massive, (tracheids +); megaspore mother cells (1-)numerous, embryo sac with chalazal caecum; pollen tube penetrates the chalazal/lateral pole of the embryo sac; fruit with accrescent leafy bracteoles [from one or two orders of branching]; nuts large to medium, not or little flattened.
4/50. N. Temperate, South East Asia, Central America.
Age. The crown-group age of Coryloideae is estimated at 87.5-70 m.y. (Forest et al. 2005), about 39-22 m.y. (Grimm & Renner 2013: preferred age, other estimates similar), or (56.4-)54(-50.6) m.y. (Xiang et al. 2014).
Synonymy: Carpinaceae Vest, Corylaceae Mirbel
Evolution: Divergence & Distribution. For an increase in diversification rate in the family, perhaps triggered by the aquisition of the deciduous habit, see Bouchenak-Khelladi et al. (2015).
Ecology & Physiology. Betula grows with other ECM trees in the boreal forest, and it can also be a major component of the biomass in tundra vegetation (Chapin & Körner 1995). Alnus can be common in neotropical montane forests, A. acuminata dominating in montane cloud forests of the Yungas at 1500-3000 m altitude to about 28o S. (Peay 2016; Wicaksono et al. 2017).
Alnus is well known as a N-fixing plant, and is used in land remediation. The co-occurrence of nitrogen fixation and the ECM habit is rather unusual (but see Fabaceae), and the ECM fungi may also help enhance phosphorus acquisition by the plant (Walker et al. 2013). Cluster roots have been reported from the genus (Shane & Lambers 2005), although they seem to be rather sporadic in their occurence, and carboxylate exudation by the roots may help in phosphorus acquisition (Lambers et al. 2012).
Pollination Biology & Seed Dispersal. Heterodichogamy is reported from Corylus (Renner 2001 for references). In Corylus avellana in particular there may be three to five months between pollination and fertilization. Ovules start to develop about half way through this period and the developing nuts are already 7-10 mm across at the time of fertilization. If pollination does not occur, the stigma may remain receptive for up to three months (Germain 1994). See also Benson et al. (1906), for pollination, etc., of Carpinus, Nawaschin (1899) for that of Corylus, and Dahl and Fredrikson (1996), fertilization of Betula, for more information.
Plant-Animal Interactions. Leaf-mining larvae of Eriocraniidae, probably the subbasal clade in the lepidopteran Angiospermivora, eat Betulaceae (and Fagaceae: Regier et al. 2015 and references).
Bacterial/Fungal Associations. Põlme et al. (2013) reported quite an assemblage of ECM fungi, although compared with other ECM plants not that many, but they are unrelated and are rather species-specific (Bruns et al. 2002; Walker et al. 2013; Wicaksono et al. 2017); this may be connected with the tendency of Alnus to be a pioneer, and plant-fungus specificity tends to be higher in such situations (Bruns et al. 2002). Both AM and sometimes also ECM associations have been recorded here (e.g. Rose 1980), and there have been reports that Alnus may lack ECM (Michelsen et al. 1998).
Chemistry, Morphology, etc. Staminate flowers in Coryloideae are sometimes reported as being single (e.g. Mabberley 1997), however, as Abbe (1935) noted, there are usually three together. The staminate "flower" of Ostrya, with some 15 pairs of half stamens, is apparently pseudanthial in nature, also being derived from three flowers (Abbe 1935, 1974; Macdonald in Sattler 1973: see also Nothofagaceae). Betula has three carpellate flowers per bract. In staminate flowers of Corylus the perianth is reduced to a ridge. Corylus avellana has spongy endexine at the pore (Weber & Ulrich 2010). The orientation of stamens or carpels in the flower may change during development in Betula (Lin et al. 2010), while Endress (2008c) discussed the structural lability of carpellate flowers of Carpinus betulus. The ovary of Corylus is not always obviously inferior.
See Crane (1989) and Kubitzki (1993b), both general, Ashburner and McAllister (2013: Betula), Endress (1967: general, comparison with Hamamelidaceae, Corylopsis is the link), Hegnauer (1964, 1989: chemistry), Horne (1914), Heller (1935) and Abbe (1935), all flowers, inflorescences, Manchester and Chen (1998: fossils).
Phylogeny. Although R.-Q. Li et al. (2004) suggested that Betuloideae were paraphyletic, with Alnus and Betula being successively sister to the rest of the family (see also H.-L. Li et al. 2015, 2016; M. Sun et al. 2016; Z.-D. Chen et al. 2016: support very weak). However, Forest et al. (2005), analysing variation in ITS and the 5S spacer, recovered the two subfamilies above as monophyletic (see also Grimm & Renner 2013; Xiang et al. 2014; Ma et al. 2015: phyoltranscriptomic analyses).
The ITS phylogeny of Betula provided by N. Wang et al. (2016) suggests that there has been hybridization, even between species now placed in separate subgenera. The monophyly of Ostrya and Carpinus is unclear (see Yoo & Wen 2002, 2007, 2008; Xiang et al. 2014), the former genus perhaps being paraphyletic. See also Z.-D. Chen et al. (1999) for phylogeny and evolution.
Classification. The two subfamilies have sometimes been recognised as families, as by Brummitt (1992).
For a checklist and bibliography, see Govaerts and Frodin (1998: as Corylaceae and Betulaceae). For an infrageneric classification of Betula, see Ashburner and McAllister (2013), but c.f. N. Wang et al. (2016).