EXTANT SEED PLANTS
Plant woody, evergreen; nicotinic acid metabolised to trigonelline; primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins rich in guaiacyl units; true roots present, xylem exarch, branching endogenous; arbuscular mycorrhizae +; shoot apical meristem complex; stem with ectophloic eustele, endodermis 0, xylem endarch, branching exogenous; vascular tissue in t.s. discontinuous by interfascicular regions; vascular cambium + [xylem ("wood") differentiating internally, phloem externally]; wood homoxylous, tracheids +; tracheid/tracheid pits circular, bordered; sieve tube/cell plastids with starch grains; phloem fibers +; stem cork cambium superficial, root cork cambium deep seated; nodes ?; stomata ?; leaf vascular bundles collateral; leaves spiral, simple, axillary buds?, prophylls [including bracteoles] two, lateral, veins -5(-8) mm/mm2; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores] +, grains mono[ana]sulcate, exine and intine homogeneous, ovules unitegmic, crassinucellate, megaspore tetrad tetrahedral, only one megaspore develops, megasporangium indehiscent; male gametophyte development first endo- then exosporic, tube developing from distal end of grain, to ca 2 mm from receptive surface to egg, gametes two, with cell walls, with many flagellae; female gametophyte endosporic, initially syncytial, walls then surrounding individual nuclei; seeds "large", first cell wall of zygote transverse, embryo straight, endoscopic [suspensor +], short-minute, with morphological dormancy, white, cotyledons 2; plastid transmission maternal; two copies of LEAFY gene, PHY gene duplication, mitochondrial nad1 intron 2 and coxIIi3 intron present.
MAGNOLIOPHYTA Back to Main Tree
Plant woody, evergreen; lignans, O-methyl flavonols, dihydroflavonols, triterpenoid oleanane, non-hydrolysable tannins, quercetin and/or kaempferol +, apigenin and/or luteolin scattered, cyanogenesis via tyrosine pathway [ANITA grade?], lignins derived from both coniferyl and sinapyl alcohols, containing syringaldehyde [in positive Maüle reaction, syringyl:guaiacyl ratio less than 2-2.5:1], and hemicelluloses as xyloglucans; root apical meristem intermediate-open; root vascular tissue oligarch [di- to pentarch], lateral roots arise opposite or immediately to the side of [when diarch] xylem poles; origin of epidermis with no clear pattern [probably from inner layer of root cap], trichoblasts [differentiated root hair-forming cells] 0; stem with 2-layered tunica-corpus construction; wood fibers and wood parenchyma +; reaction wood ?, with gelatinous fibres; starch grains simple; primary cell wall mostly with pectic polysaccharides; tracheids +; sieve tubes eunucleate, with sieve plate, companion cells from same mother cell that gave rise to the tube, the sieve tube with P-proteins; nodes unilacunar; stomata with ends of guard cells level with aperture, paracytic; leaves with petiole and lamina [the latter formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, vein endings free; flowers perfect, polysymmetric, parts spiral [esp. the A], free, development in general centripetal, numbers unstable, P not differentiated, outer members not enclosing the rest of the bud, smaller than inner members, A many, with a single trace, introrse, filaments stout, anther ± embedded in the filament, tetrasporangiate, dithecal, with at least outer secondary parietal cells dividing, each theca dehiscing longitudinally by action of hypodermal endothecium, endothecial cells elongated at right angles to long axis of anther, tapetum glandular, binucleate, microspore mother cells in a block, microsporogenesis successive, walls developing by centripetal furrowing, pollen subspherical, binucleate at dispersal, trinucleate eventually, tectum continuous or microperforate, exine columellar, endexine thin, compact, lamellate only in the apertural regions, pollen germinating in less than 3 hours, tube elongated, growing at 80-600 µm/hour, with callose plugs and callose-based walls, penetrating between cells, siphonogamy, penetration of ovules within ca 18 hours, distance to first ovule 1.1.-2.1 mm, nectary 0, G free, several, ascidiate, with postgenital occlusion by secretion, few [?1] ovules/carpel, ovules marginal, anatropous, bitegmic, [outer integument often largely subdermal in origin, inner integument dermal], micropyle endostomal, integuments 2-3 cells thick, megasporocyte single, megaspore lacking sporopollenin and cuticle, chalazal, female gametophyte ?type, stylulus short, hollow, stigma ± decurrent, wet [secretory]; P deciduous in fruit; seed exotestal; double fertilisation +, endosperm ?diploid, cellular [first division oblique, micropylar end initially with a single large cell, chalazal end more actively dividing], copious, oily and/or proteinaceous, embryo cellular ab initio; germination hypogeal, seedlings/young plants sympodial; Arabidopsis-type telomeres [(TTTAGGG)n]; whole genome duplication, single copy of LEAFY and RPB2 gene, knox genes extensively duplicated [A1-A4], AP1/FUL gene, paleo AP3 and PI genes [paralogous B-class genes] +, with "DEAER" motif, SEP3/LOFSEP and PHYA/PHYC gene pairs.
Warning: some of the more cryptic characters have been observed in relatively few taxa in the pectinations basal to the [magnoliid + monocot + eudicot + Chloranthaceae] group.
Possible apomorphies are in bold. On the Cycadales page there is further discussion of relationships between the major clades of seed plants; for some characters, whether or not they are apomorphies of angiosperms will depend on relationships between extant gymnosperms. The balance of evidence seems to be tilting towards the hypothesis that extant gymnosperms are sister to angiosperms, however, given the uncertainty in our knowledge of the relationships between the five major seed-plant clades, direct links are provided to the four other clades from here: Cycadales, Ginkgoales, Gnetales, and Pinales, and also to the general discussion under seed plant evolution.
Thermogenic (beetle) pollination mechanisms occur in some members of many "basal" lineages, including Araceae, although not Laurales, Amborellales, and Acorales (Thien et al. 2000; see also Seymour et al. 2003 for functional explanation of thermogenesis). Beetles are common pollinators, but bees are not conspicuous.
Root morphology, cork development, etc., are unknown in Amborellaceae, an absence of knowledge complicated by the very distinctive "aquatic" morphology and anatomy of the next clade up, Nymphaeales. As to other characters of possible phylogenetic interest, the triperpenoid oleanane is widely distributed in angiosperms, but in no other extant seed plants (Taylor et al. 2006). The mycorrhizal condition of the ANITA grade (Amborellales, Nymphaeales and Austrobaileyales here) is largely unknown, as is that of Canellales, Piperales, and most of Laurales, although mycorrhizae are absent in Nymphaeales (and Ceratophyllales), as might be expected for aquatic groups (Landis et al. 2002; Wang & Qiu 2006). Magnoliophyta as a whole are likely to have vesicular-arbuscular mycorrhizae, indeed, this may be a much more "basal" character, and it is placed here as a commonality of all extant seed plants. Boyce at al. (2004) discuss interesting variation in the lignification of the primary cell wall; it is slight in "basal" angiosperms (and also in Drimys, a magnoliid), less in eudicots, and this may have functional implications. However, the sampling is very preliminary. p-hydroxybenzaldehyde, a component of many lignins, is apparently absent from broad-leaved angiosperms - at least from magnoliids and eudicots (Towers & Gibbs 1953), but is present in the monocots sampled and in some living gymnosperms (and also some Myrtaceae, etc.). Axial parenchyma is notably slight to absent in Amborellales, Austrobaileyales, Laurales, and Chloranthales (Herendeen et al. 1999). Leaf traces make connections only with xylem produced during the first year (Tomlinson et al. 2006); cf. Pinales. Leaf teeth of the chloranthoid type, with a central vein joined by branches from above and below and then proceeding to a thickened apex, may be plesiomorphic within angiosperms and synapomorphic for them (Doyle 2007).
Endress (2001a) describes a possible plesiomorphic flower and fruit morphology for angiosperms in some detail; he notes i.a. that the carpels may have uniseriate hairs - in Trimeniaceae and Nymphaeales the apical cell of these hairs is elongated and tanniniferous. The perianth members may each have a single trace, but I haven't followed this character in the basal pectinations carefully enough. For pollen characters of angiosperms of the ANITA grade, and also magnoliids, see Doyle (2007); note that pollen morphology of Amborellaceae is still not well understood. Indeed, some of the pollen characters may be incorrectly placed on the tree. The plesiomorphic condition for embryo sac morphology and also endosperm ploidy is unclear given the recent findings of Friedman and his co-workers (see Friedman 2006 and references, also above). Routley et al. (2004) find protogyny to be very common in "basal" angiosperms (Amborellaceae inapplicable, variable in eudicots and above Alismatales in monocots - see also Endress 1994b). In Amborellaceae and some other ANITA-grade angiosperms - note, including Hydatellaceae - the stigma has multicellular papillae. Whether or not an 8-nucleate embryo sac and triploid endosperm are synapomorphies for all angiosperms or only for those angiosperms in the [magnoliid + monocot + eudicot + Chloranthaceae] group is unclear at present (Friedman 2001a, b; Baroux et al. 2002), although Friedman et al. (2003a, esp. b) and Friedman and Williams (2003, 2003) incline towards the latter hypothesis. Recent findings on the development of the 9-nucleate embryo sac of Amborella (Friedman 2006) have not really clarified the evolutionary scenarios possible. Similarly, there is much variation in microsporogenesis and pollen morphology in Nymphaeales, Amborellales, etc. (e.g. Furness et al. 2002). Lauraceae, Degeneriaceae and Magnoliaceae, at least, develop a massive, multiseriate suspensor during embryogenesis (Wardlaw 1955). Seeds of angiosperms may be notably smaller than those of extant gymnosperms (Moles et al. 2005a). Seedlings/young plants with decumbent lignotubers and sympodial growth are common in the ANITA grade and in Chloranthaceae, although they are not known in Nymphaeaceae, and early angiosperms may have been smallish trees (Feild et al. 2003, 2004; Feild & Arens 2005). Most eudicots have seedlings/young plants that are at least initially erect. Genome size in many angiosperms is small, less than 1.4 picograms in size, although there are some notable exceptions (e.g. a few Liliales and Asparagales); it is smaller than that of extant gymnosperms, although there the genomes in Gnetales are smaller than those of the others (Leitch et al. 2005: see also Suda et al. 2005 who suggest that members of the Macaronesian flora tend to have particularly small genomes). Note that at this level genome size and basic degree of ploidy seem not to be connected. Evans and Rees (1971) discuss variation in the length of the mitotic cycle, with that in eudicots being ca 4 hours longer than that in monocots (interphase, G1, is involved, 16 species sampled). For B-function genes, etc., see S. Kim et al. (2004b) Synonymization: AP3 and PI with DEF and GLO.
Relationships between members of the basal angiosperm pectinations are being clarified. Donoghue and Mathews (1998) listed 16 different hypotheses of relationships among basal angiosperms that involved the the first three nodes, but it seems that Amborellaceae are most likely to be sister to other angiosperms (not an hypothesis that Donoghue and Mathews included!), Nymphaeaceae sister to the rest, then Austrobaileyales - the ANITA grade (e.g. Mathews & Donoghue 1999; Qiu et al. 1999, 2000, 2005, 2006a, 2006b [some analyses], 2007; P. Soltis et al. 1999, 2000; Parkinson et al. 1999; Zanis et al. 2002; Magallón & Sanderson 2002; Kim et al. 2003; Borsch et al. 2003, 2005; Hilu et al. 2003; Nickerson & Drouin 2004; Aoki et al. 2004; P. Soltis & D. Soltis 2004; Müller et al. 2006a; Hansen et al. 2007). This is the topology followed here. There are also suggestions that the basal clade consist of Amborellales + Nymphaeales, perhaps favoured by analyses of mitochondrial genes (Qiu et al. 2006b: however, "it is sufficiently clear that the first diverging lineage of extant angiosperms consists of Amborella + Nymphaeales" [p. 845] seems something of an overstatement, and note that there are several unexpected if poorly supported relationships elsewhere in their prefered tree) - see also Qiu et al. (2000, 2005, 2006a), Mathews & Donoghue (2000), Graham et al. (2000), Stefanovic et al. (2004), Leebens-Mack et al. (2005), Cai et al. (2006), and some trees in Jansen et al. (2006b), Bausher et al. (2006), Chang et al. (2006) and Wu et al. (2007). Soltis et al. (2007; data from D. Soltis et al. 2000) found that the relationships obtained depended on the method of analysis; Bayesian analysis favoured [Amborellaceae + Nymphaeaceae], while parsimony yielded Amborellaceae as sister to the rest. (Remember, too, that different seed plant topologies were obtained from analyses using single genes or the same number of sites chosen from twelve separate loci [Burleigh & Mathews 2007a], and maximum likelihood and maximum parsimony were susceptible to systematic error in an analysis of a twelve locus data set [Burleigh & Mathews 2007b].) On balance, however, Amborella alone being sister to all other extant angiosperms seems most likely. For other studies, see Ruhlman et al. (2007), Jansen et al. (2007) and Moore et al. (2007).
There are other possibilities. In a fairly recent study (Goremykin et al. 2003a) using complete chloroplast sequences, but for only 10 angiosperms, suggested the relationships [[[Amborellaceae + Calycanthaceae] [eudicots]] [monocots (= Poaceae only!)]], but poor taxonomic sampling with resultant long-branch attraction may be responsible for these results (D. Soltis & P. Soltis 2004; Jansen et al. 2004; Stefanovic et al. 2004; T. Degtjareva et al. 2004; D. Soltis et al. 2004). Goremykin et al. (2004) found the same general result when adding Nymphaea to their analysis; it linked with Amborella - which was still not sister to all other angiosperms. However, this study, too, suffers from the same basic sampling problem; grasses are highly derived monocots (see Kuhl et al. 2004 for the very distinct genome of Poaceae). Indeed, even when looking at complete chloroplast sequences of just a few flowering plants, the inclusion of Acorus, breaking up the long branch leading to Poaceae, had a major effect (Stefanovic et al. 2004), although there are also questions about the models used in the analyses (Lockhart & Penny 2005; Goremykin et al. 2005) and the jury may still be out (Goremykin et al. 2005): The monocots included in this last analysis did not always form a monophyletic group. Indeed, the non-monophyly of the monocots is a rather unlikely result that has been obtained in some studies where the nuclear gene 18S has been included (Troitsky et al. 1991: see Duvall et al. 2006 for references). Sampling strategies may well be critical, and this general issue has become particularly important in these analyses using relatively few taxa but for which each has relatively massive amounts of data. In some cases large amounts of data may indeed be the solution, in others, perhaps quite surprisingly little data per taxon but improved sampling will do the trick (e.g. Rokas et al. 2005; Hedtke et al. 2006), and exactly where sampling should be inceased is important (Geuten et al. 2007), although each situation will have to be evaluated independently. The recent discovery of an association of Hydatellaceae with Nymphaeales (Saarela et al. 2006) unexpectly allows sampling in this area of the tree to be improved; it will be interesting to see if inclusion of members of this taxon affect the topology and support values of the basal part of the angiosperm tree. Finally, some kinds of DNA data may be positively misleading when it comes to understanding relationships (Duvall & Ervin 2004; Qiu et al. 2005; Duvall et al. 2006, 2008b; G. Petersen et al. 2006b), with horizontal transfer being notably common in mitochondrial genomes (Sanchez-Puerta et al. 2008, cf. Cusimano et al. 2008).
Within angiosperms, there are convenient summaries of the copious literature on relationships between the major clades in e.g. P. Soltis & D. Soltis (2004), D. Soltis et al. (2005b) and Qiu et al. (2005). There is additional literature cited at individual nodes, see especially the notes immediately preceding the Magnoliales, i.e. the magnoliid clade, and Acorales (both the [monocot + eudicot] clade and monocots themselves), Ranunculales (eudicots), Berberidopsidales (core eudicots), and Cornales (asterids). The discussion below is based on the usually rather conservative topologies of the trees in this site.
Synonymy: Magnoliophytina Reveal - Magnoliophyta Reveal
EVOLUTION OF FLOWERING PLANTS (very much under construction - indeed, the account on the Students page is much more readable...)
When thinking about diversification, dating is crucial. Age estimates for orders, families, etc., can be found on the appropriate pages, but they should all be treated with extreme caution. The whole issue of dating is a subject of intense discussion (e.g. Pirie et al. 2005; Bell & Donoghue 2005; Magallón & Sanderson 2005). Clade ages are unreliable at this stage of our knowledge, and in several cases there are substantially different estimates for the same event (e.g. see Magallón et al. 1999; Magallón and Sanderson 2001; Wikström et al. 2001, 2004; Davies et al. 2004: diversification rates in the context of a dated supertree; Magallón 2004: general problems in dating, literature; Sanderson et al. 2004: molecular dating; Crepet et al. 2004: paleontological dating; etc.).
The relationships of angiosperms to other seed plants and the whens, whys and wherefores of their diversification remain an abominable mystery (see Davies et al. 2004b; Friis et al. 2005). Suggestions as to the time of origin of the clade now represented by angiosperms alone range from the Triassic to the late Jurassic, although a distinction needs to be made between 1) the origin of the clade of which angiosperms are the only extant representative, i.e. stem angiosperms (probably most will have been gymnospermous), 2) the origin of plants with carpels, tepals, and a heterosporangiate strobilus, i.e. angiosperms in general, and 3) the origin of crown angiosperms, i.e. flowering plants as we know them; the Triassic-Jurassic age just mentioned refers to these latter.
Stem angiosperms presumably are early Carboniferous or before, 350±35-305-275±35 million years old, if the angiosperm clade is sister to the clade including all living gymnosperms (e.g. Savard et al. 1994; Crane et al. 1995; Goremykin et al. 1997; Crane 1999), or even just to Pinales, to a younger bound of Permian in age (Doyle 1998a). For the bulk of their some 100 million years plus history stem angiosperms will probably have lacked flowers and even carpels and will have had naked seeds and other features of the extant gymnosperms (cf. mammal-like reptiles and mammals); it has recently been suggested (Wang et al. 2007) that the early Jurassic Schmeissneria, previously placed in Ginkgoales, is angiospermous, with closed carpels (see origin 2 above), although it is difficult to see this in the fossils. Cycadeoids or Bennettitales - "fossil beehives" - have long been associated with angiosperms (see also Doyle 2006 and Hilton & Bateman 2006 for recent cladistic analyses and entry into the older literature). Individual ovules are radiospermic and lack a cupule, they have a vascularised nucellus but not a vascularized integument, and seeds with an outer sarcotesta, a sclerotestsa, and a layer inside that (Rothwell & Stockey 2002). Oleanane distribution is consistent with this relationship (Taylor et al. 2006). (For further discussion, see seed plant evolution.) Note, however, that cycadophytes include Bennettitales and Cycadales, and there are similarities in wood anatomy characterizing this group (see Cycadales page, Ryberg et al. 2007).
Estimates of the age of crown-group angiosperms are in the range (130-)140-180(-210) million years before present (e.g. Doyle 2001; Sanderson & Doyle 2001; Wikström et al. 2001; Soltis et al. 2002a; Aoki et al. 2004; Sanderson et al. 2004; Bell et al. 2005; Leebens-Mack et al. 2005; Moore et al. 2007). Estimates based on molecular data tend to be substantially older than others, Magllón (2008 and references) noting times of 182-158 million years before present for the basal split within angiosperms, i.e. Lower to Middle Jurassic, with eudicots appearing in the uppermost Jurassic. However, there is a disparity with the plant fossil record, unambiguous angiosperm fossils from before the lower Cretaceous being at best few, perhaps the oldest remains of the clade being pollen from the Valanginian-Hauterivian (132-141 million years before present). If columellate pollen is ancestral in angiosperms (but see above), there may be connections with the Triassic reticular-columellar Crinopolles pollen (Doyle 2001; Zavada 2007). The description of Archaefructus, herbs that were probably aquatics and living at least 124 million years old (Sun et al. 2002), is of some interest. Archaefructus has been interpreted as having perfect flowers that are unlike those of extant angiosperms - there is no perianth, the receptacle is very elongated, the stamens are paired, and the carpels are conduplicate. It is unclear how it relates to extant angiosperms, but it is unlikely to be sister to all angiosperms - indeed, its flowers are perhaps better interpreted as inflorescences, the paired stamens then representing bistaminate staminate flowers (see Zhou et al. 2003; Friis et al. 2003b; Ji et al. 2004; Doyle & Endress 2007; also Crepet et al. 2004 for a critical analysis of this and other early fossil angiosperms). Hyrcantha, also more or less aquatic, has been described from these deposits (Dilcher et al. 2007); it has ochreate leaves and partly connate carpels with apparent resin obdies at their apices. Perhaps more remarkably, fossils ascribed to Sarraceniaceae have been described from deposits about the same age (Li 2005), while fossils of Nelumbonaceae - as Nelumbites, the leaves with rather different venation but the flowers with an expanded floral receptacle - have been reported from the early Cretaceous in the mid to late Albian (Upchurch & Wolfe 2005).
Since the sister taxon to the angiosperms remains conjectural (Archaefructus by itself is not clarifying the problem much) and the Nymphaeales are highly autapomorphic (in some respects) aquatics, polarity of many angiosperm characters is unclear (see also Friedman & Floyd 2001; Ronse De Craene et al. 2003). It has been suggested that there are similarities between the ovules of some Magnoliaceae and the cupules of Caytonia (e.g. Umeda et al. 1994), but these are probably superficial, and features like lobing of the integuments seem to have little systematic significance, certainly there is no suggestion that the two integuments are of fundamentally different nature (Endress & Igersheim 2000; Endress 2005c). There are changes in the life cycle. Extant angiosperms seem to have a relatively shorter time between pollination and seed dispersal, although the embryos of Amborella, etc., are still minute when the fruit is ripe. Furthermore, angiosperms as a whole tend to become mature at a younger age than do gymnosperms, and this may aid diversification (Verdú 2002: note, taxa from the ANITA grade were not included in the analysis). If the relationships suggested by Sun et al. (2002) are confirmed, then changes to polarities are to be expected. See also the Warning above!
Diversification of angiosperms was well under way by 137 million years before present, but there seems to be a gap of ca 30 million years or more before crown group diversification started (Feild & Arens 2005). Indeed, although the evolution of the flower that characterises angiosperms is considered a critical event (e.g. Dilcher 2000), diversification in terms of rapid increase in species number or assumption of ecological dominance seems not to have occured immediately (see Sanderson & Donoghue 1994, although in the context of a rather diferent topology). Nevertheless, there is a wealth of angiosperm fossil material from the Early Cretaceous, for instance, there are some 140-150 taxa from the Barremian-Aptian ca 125 million years before present in Portugal alone. Nearly all these remain unassigned to extant families, although recently, pollen of a comparable age (120-110 million years before present) has been fairly safely identified as belonging to Araceae-Pothoideae (Friis et al. 2004). 85% of these Barremian-Aptian fossils are from plants of the magnoliid grade or from monocots (Friis et al. 2001), and many of these represent rather small plants and have rather small flowers, even if derived morphologies such as inferior ovaries or whorled parts, etc., appear early (e.g. Crane et al. 1995; Doyle 1999; Eklund 1999; Friis et al. 2000 for literature). Doyle (2001) notes the abundance of fossils with ascidiate carpels and exotestal seeds in these floras - and in extant members of the ANITA grade (Amborellales, Nymphaeales, Austrobaileyales) and Chloranthaceae. In general, many of these older plant fossils have character combinations unlike those of any extant family, even if they seem close to them. However, the major groups of monocots, asterids, and rosids were all probably diverging by the earlier part of the Cretaceous (Sanderson et al. 2004).
Early angiosperms may have been smallish tropical trees rather tolerant of shade and disturbed conditions (Feild et al. 2003, 2004; Feild & Arens 2005). Vessels may have evolved in such plants growing in humid conditions (Feild 2005). Seeds of angiosperms may be notably smaller than those of extant gymnosperms (Moles et al. 2005a), and if early angiosperms were relatively small plants, this is to be expected, since plant and seed size are quite strongly linked (Moles et al. 2005b). There are also suggestions that the origin of angiosperms occured in a wet or aquatic habitat, or at least that early angiosperms favoured such habitats (Qiu et al. 2006, in the context of an Amborellales + Nymphaeales clade), although this seems unlikely. There was latitudinal spread of angiosperms - and a similar spread of increasing density and abundance - over a period of about 49 million years from the initial appearance of angiosperms in more tropical environments (Axelrod 1959; see Wing & Boucher 1998 for further references). Major diversification of angiosperms and their replacement of free-sporing plants (i.e., not including conifers, although cycads seem to have declined) occured in North America in the Albian-Turonian, ca 100 million years ago, although again slightly later at higher latitudes (e.g. Crane & Lidgard 1988; Lidgard & Crane 1988; Wing & Boucher 1998; Lupia et al. 1999). Crane and Herendeen (1996) note that taxa referable to extant angiosperm families appear in the fossil record in east North America around 115-90 million years ago, and by some 85 million years ago the diversity had increased considerably (see also Lidgard & Crane 1988, etc.); insect pollination was evident by the Turonian ca 90 million years before present (see below). Wing and Boucher (1998) discuss Cretaceous angiosperm ecology (in the context of the anthophyte hypthesis of their relationships, but see above), concluding that by the end of the Cretaceous diversification of flowering plants represented "the evolution of a highly speciose clade of weeds but not necessarily a major change in global vegetation" (Wing & Boucher 1998, p. 379). Through much of the Cretaceous, dominance of angiosperms tended to be restricted to fluvial or disturbed environments, although diversity was sometimes quite high towards the end of this period. Even if gymnosperm - or at least conifer - diversity seems to have been relatively unaffected by the increasing diversity of angiosperms (e.g. Wing & Boucher 1998), the former do seem to have become more restricted in terms of areas where they remained common, and ecological factors such as slow seedling growth and leaf construction, etc., can be adduced to explain this change (e.g. Bond 1989).
Diversification of angiosperms is associated with that of insects, indeed, with diversification of just about all elements of the biota. Associations between extant plants and many insects are close, whether the insects are herbivores, detritivores, or pollinators. Although there have been suggestions that it is not so much increased diversification but reduced extinction that has characterised the evolution of insects (Labandeira & Sepkoski 1994), this is unlikely, and diversification of angiosperms appears to be contemporaneous with the massive diversification of many insect groups that are now more or less dependent on them; plant-feeding insects make up at least one quarter of all described species (Janz et al. 2006). The phytophagous sister taxa Curculionoidea and Chrysomeloidea, including about half of all herbivorous insects, seem to diversify in parallel with angiosperms (Farrell 1998), even if a number of not very speciose but old clades of these insect groups are found on gymnosperms, including cycads. This association dates back to the Jurassic or earlier (e.g. Labandeira et al. 1994), although Oberprieler (2004) suggests that the current associations of beetles with the cycads that they pollinate are recent. (Of course, there are also very species rich beetle clades that are not associated with plants, e.g. Barraclough et al. [1998]). All told, the bulk of these phytophagous beetles, well over 100,000 species altogether and in some five clades, are found on angiosperms and may have diversified since the early Cretaceous (Farrell 1998), perhaps diversifying first on monocots and then moving on to broad-leaved angiosperms (Reid 2000). Of the over 100,000 species of herbivorous Coleoptera, about two thirds are mono- or oligophagous, while slightly under 100,000 species of Lepidoptera are herbivores, of which some three quarters are mono- or oligophagous (Bernays & Chapman 1994). Similar patterns are evident at the level of individual groups like the bark weevils (Scolytinae), which are less speciose in clades that returned to conifers, and also the weevils that make tunnels in the bark and are associated with the ambrosia fungi (Ophiostoma, Ceratocystis: Ophiostomatales, ascomycetes). This association has evolved about seven times and, like other examples of the adoption of agriculture by insects, is unreversed (Farrell et al. 2001; Mueller et al. 2005). Ants, almost 12,000 species, also seem to have diversified after the evolution of the angiosperms, although the main clades may have diverged somewhat before; major diversification began in the late Cretaceous-early Eocene 75-50 million years before present, but ants began to be ecologically dominant only in the Eocene (there is some argument over this, but general agreement over the main timing of diversification: Hocking 1975; Grimaldi & Agosti 2000; Moreau et al. 2006; Brady et al. 2007; see also Wilson & Holldöbler 2005). Sugar obtained either directly or indirectly from plants is an important food/energy source for many ants, while plant material in general presents a great variety of resources for them; elaiosomes on seeds or fruits are found in many plants (Beattie 1985), and their appearance in clades such as Polygalaceae-Polygaleae seems to be associated with diversification (Forest et al. 2007b). There are over 4,000 species of Aphididae feeding on plant sap; again, diversification was Late Cretaceous/early Tertiary (von Dohlen & Moran 2000). Another food source for insects is rotting fruit, which presents a challenge because of its alcohol content, since alcohol is toxic. This food "niche" was exploited by particular groups of flies, particularly by Drosophilinae, some of the relationships between particular fruits and flies is very close (Ashburner 1998 [on alcohol dehdrogenase in flies]; Harry et al. 1996, 1998 [fig-breeding Lissocephala]).
Understanding details of the patterns of associations between plant and insect groups is not easy, most plant secondary metabolites showing considerable homoplasy, although there are examples of rather close associations - loose coevolution (Ehrlich & Raven 1964; cf. Janzen 1980) - that are documented on the individual order pages immediately after the "field diagnoses" of orders or families. What attracts an egg-depositing insect to one plant and prevents it laying eggs on another may be some aspect of plant chemistry (see Bernays & Chapman 1995 for host plant selection). A number of organisms sequester secondary metabolites in the larva and/or adult stages, ensuring some measure of protection by so doing, or they use the metabolites for pheromones, or these metabolites simply act as oviposition cues, appearing not to be otherwise utilised by the insect (Nishida 2002 for a review). Within herbivores, there is a general decrease in host specificity both in temperate and tropical regions and following the same general sequence, granivores > leaf miners > fructivores > leaf chewers = sap suckers > wood eaters > root feeders (Novotny & Basset 2005). Indeed, how insect larvae feed, i.e., whether they are stem borers, whether they can tolerate raphides, or latex, etc., may be more conserved than associations between larvae and particular groups of plants, and internal feeders tend to show greater phylogenetic conservatism than other types of feeders (e.g. Powell 1980; Peigler 1986; Powell et al. 1999 and references for associations with latex-containing plants; Farrell et al. 1991; Farrell & Sequiera 2001; Lopez-Vaamonde et al. 2003, 2006). Furthermore, phylogenetic conservatism may be greater in groups in which the adults tend to remain close to plants in which they grew up, as tends to happen with beetles, compared to the situation where the adult may fly away, as in many lepidoptera (Berenbaum & Passoa 1999).
Dioecious plants tend to be wind pollinated and have small flowers. If insect-pollinated, the floral displays tend to be dimorphic, those of the staminate plants being showier and so more visited; extinction is thus perhaps more likely (but Amborella...), and dioecious clades in general are not notably speciose (Heilbuth 2000; Vamosi & Otto 2002). Clades in which wind pollination is dominant are also not notably speciose, even if those clades are ecologically locally dominating, as with many Fagales; an exception is the very speciose Poaceae. Adoption of pollination of perfect flowers by animals is often associated with the success of angiosperms. Although beetle and moth pollination is known from gymnosperms (Kato & Inoue 1994; Schneider et al. 2002; Oberprieler 2004: note that dioecy is common) and angiosperms, the evolution of bees is of particular importance, given the close involvement of many of them with angiosperm pollination. Bees diversified in the early to mid Cretaceous, short-tongued bees perhaps forming a basal grade; host plant specificity of such bees may have facilitated early angiosperm evolution (Sipes et al. 2006). In the New World, the notably long-tongued euglossine bees are important polinators (the tongue is 15-42 mm long). They are vigorous fliers, and trap-line the plants they visit which are often steady-state flowerers of the understory (Janzen 1971; Ackerman 1985; Borrell 2005); plant families particularly involved include Bignoniaceae, Gesneriaceae-Gesnerioideae, Lecythidaceae-Lecythidoideae, Orchidaceae-Epidendroideae, and Zingiberales (especially Marantaceae), also Apocynaceae, Convolvulaceae, Fabaceae, and Rubiaceae. Nectar, pollen, and for the males, fragrances, are attractants. Bumblebees appear to have an innate preference for monosymmetric flowers, whereas honeybees, lepidoptera and beetles, at least, prefer polysymmetric flowers (Leppik 1957; Kalisz et al. 2006: although Rodríguez et al. 2004 found bumblebees preferred monosymmetric flowers, this was only against asymmetric flowers). Lepidoptera prefer radiate flowers, polysymmetric flowers with a definite meristicity signal, with enclosed nectar, honey bees radiate flowers with relatively accessable nectar, and beetles, etc., like flowers lacking definite symmetry signals (Leppik 1957). Fused corollas and nectaries are known from plant fossils of Cenomanian age (mid Cretaceous), inferior ovaries from late Cretaceous, zygomorphy and other pollination-related innovations from the early Tertiary (Crepet et al. 1991; Dilcher 2000). Diversification, like the devil, is in the details. Successful pollination entails the pollinator following a more or less complex and specific set of cues. Colouring of the corolla in particular, in terms of pigment type, amount, and pattern of deposition, seems to be under the control of a small family or regulatory genes in a diverse set of angiosperms (Schwinn et al. 2006). Individual groups of bees may be particularly important. Thus the euglossine bees, all neotropical, although only some 160 species, are implicated as the sole or major pollinators of many Zingiberales, Gesneriaceae-Gesnerioideae, Orchidaceae-Epidendroideae (here the males pollinate, looking for fragrances), etc. (Wiehler 1976; Williams 1982).
In general, plant and insect diversity are positively correlated in the current biota, although Hawkins and Porter (2003, see also references) note that the correlation may well not be causal. There are also correlations with temperature, with more herbivory occuring at higher temperatures, as is evident at least locally in the fossil record (Wilf & Labandeira 1999). Novotny et al. (2006) suggest that individual species of temperate and tropical plants (controlled for phylogenetic relationships) support a similar number of insect species, however, there are of course many more species of plants, and hence of insects, in the tropics. South America in particular is very diverse in both plants and insects, and this link may be evident as far back as the early Eocene, the diversity of herbivore damage in a fossil flora from Argentina being appreciably greater than in comparable North American floras (Wilf et al. 2005).
It is very easy to overemphasize links between the diversification of plants and that of insects (or other organisms) by simply forgetting cases where there is no obvious correlation.... Hardly surprisingly, our understanding of the ecological-evolutionary connections between insects and plants remains unclear; there is no simple underlying theory to explain the diversity of the interactions (Futuyma 1983). As Grimaldi and Engel (2005: p. 625) note, "Despite the fact that the mechanism is obscure as to how insects diversified with angiosperms, the overall patterns are extremely clear that the angiosperm radiations had a profound impact on insects, and vice versa." Even if initially diversification of insects and angiosperms was associated, some subsequent bouts of diversification may have occured well after the appropriate angiosperm host clades originated (implicit in Futuyma 1983; see Funk et al. 1995; Percy et al. 2004; Lopez-Vaamonde 2006), diversification of insect groups occuring - and overall diversity increasing - after they adopt new hosts (Janz et al. 2006), however, Kergoat et al. (2005) suggest that diversification of bruchids and Fabaceae may have occured more or less contemporaneously. In general, close co-evolution seems to be the exception rather than the rule, and is most evident in shallow rather than deep clades (Berenbaum & Passoa 1999 for references; cf. Farrell & Mitter 1998); looser "co-evolution", with host shifts associated with taxonomy, may be more common (see Futuyma & Mitter 1996). In any event, insects perhaps rarely act as selective agents on their hosts (Strong et al. 1983).
The end of the Cretaceous and beginning of the Tertiary may be a particularly important period in the diversification of angiosperms. There are suggestive links between the appearance of derived floral characteristics in the fossil record and the diversification of insects involved in pollination (e.g. Crepet 1985; Thompson 1994; Crepet & Fries 1997; Grimaldi 1999, etc.); the mid-Cretaceous and again the late Cretaceous/early Tertiary seem to be critical times. Although such an association by itself may be neither sufficient nor necessary to explain angiosperm diversification (Gorelick 2001, but cf. Grimaldi & Engel 2005), there are clearly connections. The end-Cretaceous bolide impact ca 65.5 million years ago with up to 80% plant species loss, at least locally, and the concomitant extinction of diet-specific herbivore insects (Labandeira et al. 2002), must also not be forgotten. Although important elements that currently make up tropical rain forests seem to have appeared in the later Cretaceous some 114 million years before present (119.4-101.1 million years before present: Davis et al. 2005a), major clades in Ericales and Malpighiales, two groups particularly notable as small trees in the tropical rainforests of today, diversifying then, and epiphytic ferns may have diversified with them (Schuettpelz 2006), tropical forests as we think of them are more probably a Tertiary phenomenon. Only with the early Tertiary does the vegetation take on a more modern appearance (Wing 1987; Burnham & Johnson 2004; Pennington et al. 2006). The bolide seems to have has a major effect on the vevgetation in many places. Indeed, in New Zealand the iridium anomaly was followed by a thin layer high in fungal remains, and in both hemispheres there are fern spikes (and, in the Netherlands, bryophytes) after the impact (Vajda & McLoughlin 2007 and references). Vegetational recovery was rapid, however, perhaps taking only a few thousands years (Vajda & McLoughlin 2007) and there seems to be a short gap between the disappearance of the dinosaurs and the evolution of mammal- and bird-dispersed fruits. The large, nutritious seeds (or large dispersal units in general) and fleshy fruits that become particularly notable in early Tertiary angiosperms are likely to have been dispersed by animals, and by mammals, birds, and bats in particular. Seed mass of angiosperms, initially rather low, increased markedly towards the end of the Cretaceous/early Tertiary 85-60 million years before present, and this change seems to be linked with a change in growth form; angiosperms now came to dominate the forests (Tiffney 1984; Moles et al. 2005b). Large seeds are common in plants that at least initially grow in shaded habitats, although they may also be favoured by dry conditions, or soils with low mineral nutrients, etc. (Leishman et al. 2000; Bolmgren & Eriksson 2005). Large seeds are also often associated with fleshy "fruits" that attract dispersal agents, and these agents, mammals and birds, also began diversifying (see above). As another factor to consider, there also seems to have been a change in the general conductive efficiency of angiosperm woods around this period (Wheeler & Baas 1991).
Diversification of seed-dispersing animals, including birds, and of the plants they dispersed may have proceeded roughly in parallel, although with something of a lag for the animals (e.g. Tiffney 1984; Wing & Tiffney 1987; Dilcher 2000; Collinson & Hooker 1991). Along with a shift in ecology, there may have been a shift in defence (see above), and perhaps also in associated herbivores. Herbivorous beetles in particular and insects in general diversified in the later Paleocene-Eocene (Farrell 1998; Wilf & Labandeira 1999; Wilf et al. 2001; Lopez-Vaaamonde et al. 2006). Diversification of of Nymphalidae-Nymphalinae seems to be a post K/T boundary phenomenon, occuring 65-33 million years before present (Wahlberg 2006), and the same is true of N.-Papilioninae (Zakharov et al. 2004); diversification may have begun before, as in Pieridae which began diversifying the the Late Cretaceous ([112-]95[-82] million years before present: Braby et al. 2006), but again, the bulk of the diversification seems to have been Tertiary. caterpillars of these group tend to show rather high food-plant specificity, and the adults may be involved pollination. However, not all post-impact floras behaved the same; there are some from ca 64 million years before present (early Palaeocene) in the western interior United States with low plant diversity (species deciduous, with thin leaves and low defences) and high diversity of insect damage, and others more diverse and with the facies of tropical fainforest (tough, thick, tanniniferous leaves) but with low diversity of herbivore damage (Wilf et al. 2006). Diversity in the tropics may have peaked in the Eocene, perhaps even topping today's levels, but the plants and ecological conditions involved may have been rather different from those of today (Jaramillo et al. 2006; see Morley 2000 for a good general account of the evolution of rainforests).
Pollination, especially by insects, but also bats and other mammals as well as birds, and seed dispersal, especially by mammals and birds, may interact, in that both may increase outcrossing. They allow for the wide dispersal of the rather large propagules and also for the pollination of the rather widely dispersed individuals that produced them (e.g. Regal 1977). Trees have a distinctive evolutionary rhythm, speciating rather slowly, in any one species the number of individuals may be quite large, and although they may be rather dispersed they are long-lived, the species themselves also being rather long-lived (Petit & Hampe 2006).
Interestingly, pioneer plants - perhaps including early angiosperms - may be able to tolerate high herbivory because they have metabolically cheap, rapidly expanding leaves with a small amount of fibers and secondary metabolites like terpenoids, phenols, and tannins; their high quality habitat allows rapid growth and low defence. Deciduous plants in general, with their short-lived leaves, tend to be eaten more than plants with long-lived xeromorphic leaves (e.g. Coley & Barone 1996; Arnold et al. 2001; Wilf et al. 2001; Lewinsohn et al. 2005). In general, one can distinguish between plants in which defence is "qualitative", the defensive compounds being highly toxic and butterfly groups like Nymphalidae being specialized herbivores, and plants with "quantitative" defence, in which the defences are more generalised - polyphenolics and the like - and where groups like Lycaenidae are the herbivores (Fielder 1996).
Phyllostomid bat diversification and that of angiosperms is also associated (Jones et al. 2005); insect-eating bats may diversify because there are more insects because of the diversity of plants, and fruit-eating bats because there is a greater diversity of fruit types. The evolution of herbivorous animals other than insects was also affected by seed plant evolution and diversification. Thus the rise and spread of grasses with their silica-rich tissues in the Miocene was followed by the explosive radiation of grazing mammals (Thomasson & Voorhies 1990). C4 photosynthesis in grasses seems to have originated in the middle Miocene, some 12.5 million years before present (Jacobs et al. 1999), and it has been suggested that the origin of this pathway affected herbivory; C4 plants tend to be less attractive to herbivorous animals because of their lower nitrogen concentration and greater amount of fibrous tissue (Caswell et al. 1973).
It is not only flowering plants and animals whose diversification seems to be associated. Within the speciose pleurocarpous mosses - about 40% of all mosses and many epiphytic - diversification seems to have been early and rapid, with subsequent semi-stasis (Shaw et al. 2003a, time of diversification unclear; Newton et al. 2006), and although there may also have been more recent ([post-]Cretaceous) diversification as well, initial radiation seems to be early in the Cretaceous and associated with the advent of angiosperms. Porellales and Jungermanniales, both leafy liverworts epiphytic on bark and leaves of flowering plants, may also have diversified since the evolution of angiosperms (Ahonen et al. 2003; Forrest & Crandall-Stotler 2004). Equisetum seems to have diverged in the Tertiary, although the clade to which it belongs has been separate from other monilophytes since the Permian, ca 250+ million years before present (Des Marais et al. 2003). A similar pattern is found within Lycopodium, where most of the diversity is the result of events within the last 80 million years at most (Wikström 2001). The diversification that gave rise to most living ferns, especially to the polypod ferns, which make up some 80% of the living fern species, may have occured subsequent to the diversification of the angiosperms through the Cretaceous and tertiary (Pryer & Schuettpelz 2007). Indeed, ferns may have temporarily dominated after the end-Cretaceous bolide impact (Schneider et al. 2004). Important elements that currently make up tropical rain forests began to diversify in the later Cretaceous some 114 million years before present (119.4-101.1 million years before present: Davis et al. 2005a), and epiphytic ferns seem to have diversified with them (Schuettpelz 2006). Diversification of extant Cycadales is apparently a Tertiary phenomenon (Oberprieler 2004).
Close relationships between seed plants and fungi, whether as mycorrhizae or endophytes, are ubiquitous (for the evolution and ecological significance of mycorrhizae, see Malloch et al. 1980; Read et al. 2000; Landis et al. 2002; etc.). Ectomycorrhizae form a Hartig net of hyphae investing rootlets and penetrating between the cortical cells; the hyphae are septate and are not intracellular - with the exceptions of Ericaceae and Orchidaceae. Although basidiomycetes are frequent in such associations, Pezizales (ascomycetes) are also quite common (Tedersoo 2006, ascomycetes with a hypogeous life style are derived from them). Ectomycorrhizae are commonly found in plants growing on nutrient-poor and organic material-rich soils, especially in temperate and tropical montane habitats, and in ectomycorrhizae such as those associated with Ericaceae nitrogen in amino acids released by the fungus is taken up by the plant. Vesicular-arbuscular mycorrhizae are formed by an association of Glomeromycota (Schüßler et al. 2001) with seed plants - found in about 70% of the latter - that is probably of very long standing (see also Baylis 1975; Redecker et al. 2000b; etc.). In vesicular-arbuscular mycorrhizae the aseptate hyphae are intracellular, often forming vesicles or branching structures called arbuscules within the cells; such associations seem to be involved in the phosphorus uptake of plants. Mycorrhizae may also affect water uptake. Although a wide variety of fungi form ectomycorrhizal associations, forests where such associations are common are not very diverse, as when Pinales, Dipterocarpaceae and relatives, some Fabaceae, or members of Fagales, all ectomycorrhizal, dominate; the reverse set of relationships hold in forests with endomycorrhizal associations (Malloch et al. 1980; Hart et al. 1989; McGuire 2007). Aquatic plants, hardly surprisingly, often lack mycorrhizae (see Radhika & Rodrigues 2007 and references for records), but the frequent absence of mycorrhizae in Caryophyllales, Proteales, etc., is interesting.
Although details of the benefits accruing to both parties are moderately well understood for some mycorrhizal and endophytic associations, this is not so for the majority of endophytic associations (e.g. Jumpponen 2001: dark septate endophytes). Endophytic fungi are found in a number of flowering plants, perhaps particularly in Poaceae (q.v.) and Ericaeae (e.g. Petrini 1986 and other references in this volume; Saikkonen et al. 2004 and references), although they are probably very widespread. Indeed, it is becoming evident that the numbers of species of fungi with endophytic associations with plants is very large, thus Arnold et al. (2001) found 418 morphospecies of endophytes in only 83 leaves of two species of tropical trees (Ouratea, Heisteria) (see also Bills & Polishook 1994; Frohlich & Hyde 1999; Arnold & Lutzoni 2007 and other articles in Ecology 88[3]. 2007). The hyphae of such endophytic fungi tend to pervade the tissues of the plant host. Transmission may occur via the seed, as in endophytic Poaceae in particular, or it may be horizontal; these associations are probably at least intermittently mutualistic (Carroll 1988, 1995).
In the tundra habitat several plants take up substantial amounts of nitrogen as amino acids directly from the soil, but the ability to do this is not obviously correlated either with mycorrhizal status or taxonomy. Thus some Cyperaceae, which lack mycorrhizae, take up N predominantly in an organic form, but others take it up in an inorganic form (Raab et al. 1999). Largely ascomycetous fine endophytes are found in plants from such habitats (Higgins et al. 2007), indeed, they may be more prevalent than arbuscular mycorrhizal fungi, since the prevalence of vesicular-arbuscular associations decreases with latitude (Olsson et al. 2004).
It is difficult to see any direct or even indirect effect of such associations, whether of fungi, insects, or other organisms, on the diversification of the plants involved. That the diversification of orb-weaving spiders, etc., is contemporaneous with that of angiosperms, or somewhat later is interesting, but probably of little effect on seed plant diversification. Along the same lines, liverworts may form associations with the same fungi that form ectomycorrhizae with the flowering plant on which the liverwort is found (Marchantia/mycorrhizal fungus/Podocarpus, the mycoheterotrophic chlorophyll-less Cryptothallus/Tulasnella/Pinus-Betula: Read et al. 2000; Bidartondo et al. 2003; Kottke & Nebel 2005 and references). The connections between such groups may be very close, but that is a separate matter.
Kier et al. (2005) describe global patterns of diversity of extant vascular plants. In general, plant diversity is broadly correlated with climate (Francis & Currie 2003: families!, but cf. Qian & Ricklefs 2004 for problems with the distribution maps used there). Details of the relationships between groups diversifying in temperature regions and their tropical relatives have been a matter of speculation for some time (e.g. Bews 1927). Thus Judd et al. (1994) found that the temperate family of temperate-tropical family pairs often arose from within the tropical family, making the latter paraphyletic. Diversification patterns in individual families may also be distinctive. For example, Davies et al. (2005) note that in Iridaceae diversification is greater in areas like southern Africa than in the northern hemisphere. Rates of molecular evolution and speciation are linked, with more molecular evolution occuring in speciose clades (Webster et al. 2003, see also Barraclough & Savolainen 2001), and there is link between environmental energy variously estimated (and this links with latitude), species richness and the rate of molecular evolution, but the connections are independent (Davies et al. 2004b, see also Allen et al. 2002, more individuals can be supported in productive environments, therefore ceteris paribus more mutations, etc.; Moser et al. 2005; Jaramillo et al. 2006). However, teasing apart historical and ecological signals in patterns of plant diversity is not at all straightforward (Ricklefs 2005).
So as to explanations for the success of the angiosperms in general, little definite can be said. Gorelick (2001) summarises some twenty hypotheses that have been advanced to explain diversification/success. It has been suggested that, given the ecological proclivities of taxa of the ANITA grade, early angiosperm evolution may have taken place in rather shaded and disturbed conditions (Feild & Arens 2005), perhaps rather different from the ecological conditions in which angiosperms prospered later. Moreover, the three clades that are successively sister to the remaining angiosperms are currently not diverse (see also Sanderson & Donoghue 1994, but working with a rather different topology), and so there appears to be no simple link between synapomorphies for angiosperms as a whole - angiospermy, perhaps the evolution of a flower, etc. - and their immediate success. Syncarpy would seem to be important, too, but it may have evolved seventeen or more times independently (a compitum also evolved in three quarters of these cases: Armbruster et al. 2002).
Any connection between gene and/or genome duplication and diversification of angiosperms is unclear. Thus S. Kim et al. (2004b) estimate the split that gave rise to the paleo AP3 and PI genes as somewhere between (297-)290-230(-213) million years before present, well before the origin of crown angiosperms. [this paragraph to be worked up.]
That being said, there are a number of large clades that can be characterised by features that seem likely to affect diversification, although the lack of firm estimates of the times of diversification in these clades remains an obstacle in understanding what has been going on. Monosymmetry is a feature of several speciose clades, and bumblebees in particular are attracted to monosymmetric flowers (see above, also gullet-type ornithophilous flowers), Kalisz et al. (2006) suggest that this is linked to the evolution of dichogamy, in particular, to that of protandry. Diversification in monosymmetric clades seems to be greater than that in their polysymmetric sister taxa (Sargent 2004, some comparisons need to be reworked), perhaps because pollinator fidelity is increased. Stebbins (1974) suggested that zygomorphy/monosymmetry had evolved more than 25 times within angiosperm families, while Westerkamp and Claßen-Bockhoff (2007) note that it is found in 38 families. However, the figure is well over three times as high (see also Endress & Matthews 2006a), although understanding just how many independent origins of monosymmetry there have been will depend critically on the evolutionary assumptions we make (e.g. Endress 1997b; Donoghue et al. 1998; Reeves et al. 2003; Cubas 2004), and as we come to know more about floral development, a clear definition of monosymmetry itself has become elusive. Nevertheless, five major clades (2000+ species each) have a preponderance of members with monosymmetric flowers - these are Orchidaceae, Zingiberales, Asteraceae, Lamiales (at the lower of the nodes where Calceolariaceae or Gesneriaceae join), and Fabaceae (of course, reversion to polysymmetric flowers has occured within these clades). But even if there are elements of common mechanisms involved in independent acquisitions of monosymmetry (Feng et al. 2006, comparing Fabaceae and Plantaginaceae), the plants in the five major clades just mentioned are ecologically/functionally very different. Thus Orchidaceae (ca 20,000 species) are ground-dwelling or epiphytic mycoheterotrophic herbs of small to moderate size producing as many as millions of tiny seeds per flower; the tepals are more or less free and the flowers, with their distinctive and complex morphologies centred on the gynostemium (cogentitally fused stamens and stigma-style) and labellum (median tepals of the inner whorl), are inverted. Insect behaviours involved in effective pollination are for the most part different from the pollen- and nectar-collecting behaviors of visitors to the other monosymmetric clades, deceit pollination being particularly common. Although the diversity of floral form in Orchidaceae is great, it is attained by variation on a rather limited basic theme. Zingiberales (2,100 species) are giant herbs of the tropics with large flowers, and their fruits usually have only a moderate number of seeds that are mostly animal dispersed. Flowers in Zingiberales vary considerably in orientation, the parts that are petaloid, number of stamens, etc. (Note that many taxa in Commelinales, sister to Zingiberales, also have monosymmetric flowers, and it is possible the the common ancestor of the two orders had such flowers.) Asteraceae (23,600 species) are also mostly herbaceous plants but with very different flowers - they are small and aggregated into capitulae, functionally each a single polysymmetric flower, and only a single seed of moderate size is produced per true flower (many per functional flower). Dispersal is often by wind. Most Lamiales (21,000 species) are more or less herbaceous plants perhaps particularly abundant oustide the tropics, although there are many tropical members which are often more or less woody; usually rather many and small seeds are produced per flower, and although some clades produce only four seeds per flower, they are still quite small, and in general dispersal is by wind. Fabaceae (19,400 species, of which 3,300 are in the secondarily polysymmetric Mimosoideae) produce rather few and relatively large seeds in the single carpel of each flower, which is inverted, the petals are more or less free, and the plants are either trees of more or less tropical forests, perhaps especially those of the neotropics, or herbs, found considerably more widely. Dispersal is either autochorous (ballistic) or animal-mediated. (Polygalaceae, with some 1,050 species the majority of which are monosymmetric, are close to Fabaceae, but the exact relationships of the two are unclear. The flowers of Polygalaceae have a gross similarity with those of Fabaceae, and again, there are only a few ovules produced per flower.) Asteraceae and Fabaceae in particular are noted for the diversity of secondary metabolites that they contain.
There are other smaller but still quite large clades in which monosymmetry is common. Campanulaceae-Lobelioideae comprise some 1,200 species of laticiferous herbs or shrubs with slit-monosymmetric flowers and dehiscent fruits with small seeds, while Caprifoliaceae s.l., comprising some 850 species, has often rather weakly monosymmetric flowers and indehiscent fruits with at most few seeds. Ericales include Lecythidaceae-Lecythidoideae with some 200 species of trees that can be a prominent element of neotropical forests. There the polystaminate androecium alone is monosymmetric, the fruit is large, and the seeds, too, are large, and consist mostly of hypocotylar tissues. In Iridaceae, one generally thinks of monosymmetry in connection with flowers of the speciose Gladiolus, for example, but from the point of view of the pollinator the flowers of Iris, Moraeaetc., are monosymmetric; a single flower consists of three meranthia each of which is strongly monosymmetric. From the insect's point of view, over half the family, 750+ species, may have monosymmetric flowers. These few clades, none particularly basal in the tree, comprise ca 2/5 of all angiosperm diversity.
Other diverse groups include Poaceae, 10,050 species of largely herbaceous wind pollinated plants that of course have very different flowers to those of the other groups mentioned (note that the adoption of abiotic pollination elsewhere is often associated with a decrease in speciation rate [e.g. Dodd et al. 1999], although not in this case). Malpighiales and Ericales, both containing a great variety of floral and fruit morphologies (monosymmetric flowers are scattered in both clades), appear to be disproportionately common among the small trees of the understory of tropical rain forests (Davis et al. 2005a).
One can also simply focus on highly speciose and recently evolved clades in general. Although Howarth and Donoghue (2004, esp. 2005) note possible connections between changes in CYC-like genes and changes in floral form in Dipsacales, direct links remain to be established - and linking these changes with diversification is yet another issue. Thus crown-group Valerianaceae may be 60-55 million years old (Bell & Donoghue 2005a), but diversification in the Andean paramo - resulting in ca 1/7 of the current diversity in the family - happened less than 5 million years ago on the arrival of Valerianaceae in that area (Bell & Donoghue 2005b) and is not associated with the evolution of particular floral (or other) "key innovations" (see also Richardson et al. 2001). The same seems to be true of Andean Lupinus species, rapid diversification there starting only some 1.76-1.19 million years before present and probably being driven by the ecological opportunities available as a result of the evolution of high altitude habitats where they are now mostly found (Hughes & Eastwood 2006). Guatteria (Annonaceae), Inga (Fabaceae- Mimosoideae) and Ocotoea (Lauraceae) between them contain over 1,000 species, all Neotropical, and the majority having evolved fairly recently (Erkens et al. 2007). Along similar lines, perhaps, Edwards and Donoghue (2006) suggest that several key elements of the cactus ecological niche were established before the evolution of the cactus life form - and subsequent diversification of the cactus clade. As Feild and Arens (2005: p. 402) observed, diversification may well depend "on the fortuitous combinations of a large repertoire of traits" rather than on any particular key innovation, and will also be much affected by the ecological opportunities available. Overall angiosperm success seems to be in considerable part the result of diversification of particular angiosperm clades, and establishing an immediate connection between acquisition of an apomorphy or group of apomorphies and diversification is difficult.
Other changes affecting diversification are best thought of outside the context of monophyletic clades, i.e., they are changes that occur in parallel. There have been major shifts in seed mass that are also rather strongly correlated with further changes in life form/plant habit, thus herbs, especially annuals, have smaller seeds and rarely have fleshy fruits; several of the large groups with monosymmetric flowers just mentioned (Lamiales, Asteraceae, Fabaceae) also include many members that are more or less short-lived herbaceous plants. Dodd et al. (1999) found that the evolution of herbs from trees to be correlated with a rise in speciation rate and the adoption of abiotic pollination with a decrease in speciation rate; Verdú (2002) suggested that is was not so much the tree habit per se that was important, but the associated condition, length of time to maturity. There are also physiological changes that may be linked to diversification. C4 photosynthesis in grasses seems to have originated in the middle Miocene, some 12.5 million years before present (Jacobs et al. 1999), and ca 50% of the 5,250+ species of the PACCAD clade alone have C4 photosynthesis. C4 photosynthesis has evolved in other clades, too, e.g. Cyperaceae, Euphoriaceae, and CAM photosynthesis is another photosynthetic variant particularly prevalent in clades like Crassulaceae, Bromeliaceae, etc. The adoption of fructans as storage polysaccharide in Poaceae-Pooideae, many Asparagales and Asterales, etc., may be linked with the ability of the plants involved to grow in seasonal climates, especially outside the tropics (Hendry 1993; Hendry & Wallace 1993).
For further discussions on diversification, see e.g. Mulcahy (1979: pollen tube competition and angiospermy), Wing and Boucher (1998: ecology), Armbruster et al. (2002: syncarpy and increase in seed set, offspring quantity, and pollen tube competition, i.e. offspring quality), Donoghue (2004: general), Gianoli (2004: climbing habit). For further discussion on woodiness, see S. Kim et al. (2004a), on the evolution of the perianth, etc., see e.g. Hasebe (1999), D. Soltis et al. (2005a, b: note that rather than thinking how often petals/a corolla has evolved, it may be more helpful to think about the evolution of a more or less sharp distinction between calyx and corolla form and function in the flower, from a condition in which there is some sort of continuum between the two), for the evolution of features of wood anatomy, see Herendeen et al. (1999: a useful table), for changes in phyllotaxy, Ronse De Craene et al. (2003), for the perianth, see Endress (2008), for the evolution of the flower and fruit, see Dilcher (2000), for variation in the embryo sac, see Friedman (2006 and references), endosperm development, see Williams and Friedman (2004 and references), and for general floral evolution in the "basal" angiosperms in particular, see Endress (2004a, b). For microsporogenesis evolution, see Doyle and Endress (2000) and especially Furness et al. (2002b) and Taylor and Osborn (2006), for pollen micromorphology, see Sampson (2000), Doyle (2005: note that the topologies of the trees on which the pollen characters are optimized are often questionable) and Taylor and Osborn (2006), for variation in seed size, see Moles et al. (2005a, b: major changes in seed mass are usually linked with changes in habit), for variation in embryo size, see Forbis et al. (2002: very useful) and Verdú (2006), and for pollen tube/male gametophyte development, see Williams (2007, 2008).
AMBORELLALES Melikian, A. V. Bobrov & Zaytzeva Main Tree, Synapomorphies.
Nodes 1:1; leaf margin toothed; plant dioecious; hypanthium +, A sessile, vascular bundle branched towards apex, pollen anaulcerate [operculum endexinous, margin poorly defined], ektexine cupulate [distinctive undulate, columella-less exine], 1 ovule/carpel, outer integument annular [cap-shaped], embryo sac 9-nucleate [three synergids], bipolar, antipodal cells die early, polar nuclei in chalazal region, stigma dry; fruit drupelets; seed coat undistinguished; endosperm triploid. - 1 family, 1 genus, 1 species.
Includes Amborellaceae.
AMBORELLACEAE Pichon, nom. cons. Back to Amborellales
Shrub or small tree; alkaloids?, plant accumulates aluminium; cork?; true tracheids +; axial parenchyma diffuse; pericycle with hippocrepiform sclereids; petiole bundles arcuate; (stomata anomocytic); leaves spiral; inflorescence cymose; flowers small, P spiral, basally connate, 5-8, single trace; staminate flowers: A 10-25, outer adnate to the base of T, vascular bundle branched near thecae; carpellate flowers: staminodes 1-2, G 5-6, whorled, ovule ± median, pendulous, hemianatropous, sessile, outer integument 4-5 cells across, micropyle endostomal; P persistent, stone surface sculpted; exotesta of polygonal thin-walled cells; n = 13; horizontal transfer of atp1 gene.
1[list]/1: Amborella trichopoda. New Caledonia. [Photo - Leaves, Flower.]
It has recently been shown that the mitochondrial genome of Amborella contains genes from a number of land plants, including at least three different mosses; such "foreign" genes may migrate to the nucleus (Bergthorsson et al. 2004). Although mitochondrial genomes like that of Amborella are as yet unknown from other angiosperms, sampling is as yet very poor.
There is no reaction wood, the stems of Amborella tending to sprawl, especially when young; in terms of architectural models (Hallé et al. 1978) the plant conforms to Troll's model. The leaves are described as being spiral at first (Cronquist 1981; Takhtajan 1997, but cf. Posluszny & Tomlinson 2003). The perianth is spiral and undifferentiated. There seems to be no agreement on the pollen morphology of Amborella; Sampson (2000) and Hesse (2001) suggest that the pollen is not really tectate (see also Doyle 2000, 2001; Doyle and Endress 2000), and the aperture type is difficult to categorise, as well as not always being present. Ovule "type" has also been variously interpreted. Friedman (2006) has recently described a very distinctive embryo sac for Amborella; the third synergid cell arises from a cell division that also produces the female gamete. In other angiosperms the polar nuclei are sister to the egg nucleus (at one end) and the central chalazal nucleus (at the other), and the egg is produced by a nuclear division; however, the overall pattern is not necessarily fundamentally different since Amborella has a 9-nucleate embryo sac (cf. Friedman 2006). But how widespread the "other angiosperm" pattern really is, is unclear, and in part it may rest on the belief that the micropylar and chalazal ends of the embryo sac are identical, each representing a single, highly reduced archegonium (e.g. Porsch 1907, note that Porsch had an "Englerian" concept of seed plant evolution, with Amentiferae being primitive. He and others at that time [e.g. Nawaschin 1895] saw chalazogamy in Amentiferae [see also Ulmaceae] as being in some way intermediate between porogamy and non-angiospermy, where the female gametophyte has more than a single archegonium). Bobrov et al. (2005) show that the drupe of Amborella differs from a typical drupe in that the bulk of the woody layer is mesocarpial in origin, unlike the drupes of Laurales, etc. Tha nature of the resinous cavities in the mesocarp is unclear; although not observed by Bobrov et al. (2005), they are unlikely to be an artefact caused by re-expansion of dried fruits prior to study. The seed coat appears to have thin, unlignified walls, as might be expected in such a fruit, although some lignification has been reported (Tobe et al. 2000). The embryo must be very small indeed; I could not see it in two drupelets that I dissected.
Additional information is taken from Bailey and Swamy (1948: general), Metcalfe (1987: anatomy), Philipson (1993), Sampson (1993: pollen), Floyd and Friedman (2000: endosperm), Carlquist and Schneider (2001: wood anatomy), Yamada et al. (2001a: ovules), Posluszny and Tomlinson (2003: floral morphology), Field et al. (2003: ecophysiology) and especially Tobe et al. (2000: embryology). Chemistry?