EXTANT SEED PLANTS
Plant woody, evergreen; nicotinic acid metabolised to trigonelline, (cyanogenesis via tyrosine pathway); primary cell walls rich in xyloglucans and/or glucomannans, 25-30% pectin [Type I walls]; lignins rich in guaiacyl units; true roots present, apex multicellular, xylem exarch, branching endogenous; arbuscular mycorrhizae +; shoot apical meristem multicellular, interface specific plasmodesmatal network; 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 mm/mm2 [mean for all non-angiosperms 1.8]; plant heterosporous, sporangia eusporangiate, on sporophylls, sporophylls aggregated in indeterminate cones/strobili; true pollen [microspores, i.e. no distal pore for release of gametes] +, 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 [N/O//A/C and P//BE lines], 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 in 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 a sieve plate and cytoplasm with P-proteins, companion cells from same mother cell that gave rise to the sieve tube; nodes unilacunar [1:?]; stomata with ends of guard cells level with pore, paracytic, outer stomatal ledges producing vestibule; leaves with petiole and lamina [the latter formed from the primordial leaf apex], development of venation acropetal, 2ndary veins pinnate, fine venation reticulate, veins (1.7-)4.1(-5.7) mm/mm2, endings free; flowers perfect, polysymmetric, parts spiral [esp. the A], free, development in general centripetal, numbers unstable; P not sharply 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, ektexine columellar, endexine thin, compact, lamellate only in the apertural regions; 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 four-celled [one-modular, nucleus of egg cell sister to one of the polar nuclei], stylulus short, hollow, stigma ± decurrent, dry [not secretory]; P deciduous in fruit; seed exotestal; 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; 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, minute; 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 + C/PHYB + E gene pairs.
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, including in Calycanthaceae, but bees are not conspicuous.
Possible apomorphies for flowering plants are in bold. Note that the actual level to which many of these features, particularly the more cryptic ones, should be assigned is unclear, because some taxa basal to the [magnoliid + monocot + eudicot] group have been surprisingly little studied, there is considerable variation between families in particular for several of these characters, and also because details of relationships among gymnosperms will affect the level at which some of these characters are pegged. For example, if reticulate-perforate pollen is optimized to the next node on the tree (see Friis et al. 2009 for a discussion), it effectively makes the pollen morphology of the common ancestor of all angiosperms ambiguous....
Chemistry, Morphology, etc. 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. Stomatal morphology in many members of the ANITA grade is notably variable (Upchurch 1984). 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. 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 has been unclear (Friedman 2001a, b, 2006; Baroux et al. 2002), although Friedman et al. (2003a, esp. b) and Friedman and Williams (2003, 2003) incline towards the latter hypothesis - see especially Friedman and Ryerson (2009). Similarly, there is much variation in microsporogenesis and pollen morphology in Nymphaeales, Amborellales, etc. (e.g. Furness et al. 2002). Sage et al. (2009) suggest that the basic condition of the angiosperm stigma may have been dry, while Staedler et al. (2009) note that the presence of an extragynoecial compitum could be an apomorphy of angiosperms - and then it would have to be lost at least twice. 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 genomes in Gnetales are smaller than those of the others (Leitch et al. 2005); 1-1.4 picograms is the estimated ancestral genome size for angiosperms (Masterson 1994; Leitch et al. 2005). 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.
Phylogeny. On both the Cycadales (see under seed plant evolution) and especially the Students page (see seed plants again!) there is further discussion about 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.
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; Duarte et al. 2008; McCoy et al. 2008). 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. What kinds of characters are analysed may also be important; Goremykin et al. (2009b) found an [Amborella + Nymphaea] clade after removing a relatively few (500) highly variable positions from the analysis. (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 (this section is being removed, so see the account on the Students page)
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 ; 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.).
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).
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).
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). If the relationships suggested by Sun et al. (2002) are confirmed, then changes to polarities are to be expected. See also the Warning above!
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).
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). 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).
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).
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). 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).
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).
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.]
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 [two-modular]; 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.]
Evolution. Stigmatic exudate may cover all the stigmas of a single flower together, and pollination of ovules in more than one carpel from pollen landing on a single stigma is possible, i.e. there is an extragynoecial compitum (Williams 2009).
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, but cf. Goremykin et al. 2009, the evidence for these tranfers perhaps questionable on methodological grounds). Although mitochondrial genomes like that of Amborella are as yet unknown from other angiosperms, sampling is as yet very poor.
Chemistry, Morphology, etc. 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. Williams (2008, 2009) describes pollen tube development and fertilization. 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.
Ovule "type" has also been variously interpreted. Friedman (2006) 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); Friedman and Ryerson (2009) discuss the evolution of the angiosperm embryo sac in detail. 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. Thus Porsch (1907) took this view, but note that he had an "Englerian" concept of seed plant evolution, with Amentiferae being primitive. Porsch and others at that time (e.g. Nawaschin 1895) saw chalazogamy in Amentiferae (see Fagales here, also Ulmaceae) as being in some way intermediate between porogamy and non-angiospermy, where the female gametophyte has more than a single archegonium.
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?
Previous Relationships. Amborellaceae were included in Laurales by Takhtajan (1981) and Takhtajan (1997).