Gnetophyta is a division of plants, grouped within the gymnosperms (which also includes conifers, cycads, and ginkgos), that consists of some 70 species across the three relict genera: Gnetum (family Gnetaceae), Welwitschia (family Welwitschiaceae), and Ephedra (family Ephedraceae). Fossilized pollen attributed to a close relative of Ephedra has been dated as far back as the Early Cretaceous. Though diverse and dominant in the Tertiary, only three families, each containing a single genus, are still alive today. The primary difference between gnetophytes and other gymnosperms is the presence of vessel elements, a system of conduits that transport water within the plant, similar to those found in flowering plants. Because of this, gnetophytes were once thought to be the closest gymnosperm relatives to flowering plants, but more recent molecular studies have largely disproven this hypothesis.
Though it is clear they are all closely related, the exact evolutionary inter-relationships between gnetophytes are unclear. Some classifications hold that all three genera should be placed in a single order (Gnetales), while other classifications say they should be distributed among three separate orders, each containing a single family and genus. Most morphological and molecular studies confirm that the genera Gnetum and Welwitschia diverged from each other more recently than they did from Ephedra.
Ecology and morphology
Unlike most biological groupings, it is difficult to find many common characteristics between all of the members of the gnetophytes. The two common characteristics most commonly used are the presence of enveloping bracts around both the ovules and microsporangia as well as a micropylar projection of the outer membrane of the ovule that produces a pollination droplet, though these are highly specific compared to the similarities between most other plant divisions. L. M. Bowe refers to the gnetophyte genera as a "bizarre and enigmatic" trio because, the gnetophytes' specialization to their respective environments is so complete that they hardly resemble each other at all. Gnetum species are mostly woody vines in tropical forests, though the best-known member of this group, Gnetum gnemon, is a tree native to western Malesia. The one remaining species of Welwitschia, Welwitschia mirabilis, native only to the dry deserts of Namibia and Angola, is a ground-hugging species with only two large strap-like leaves that grow continuously from the base throughout the plant's life. Ephedra species, known as "jointfirs" in the United States, have long slender branches which bear tiny scale-like leaves at their nodes. Infusions from these plants have been traditionally used as a stimulant, but ephedrine is a controlled substance today in many places because of the risk of harmful or even fatal overdosing.
Knowledge of gnetophyte history through fossil discovery has increased greatly since the 1980s. Gnetophyte fossils have been found that date from the Permian and the Triassic. Fossils dating back to the Jurassic have been found, though whether or not they belong to the gnetophytes is uncertain. Overall, the fossil record is richest in the early Cretaceous, with fossils of plants, seeds, and pollen have been found that can clearly be assigned to the gnetophytes.
With just three well-defined genera within an entire division, there still is understandable difficulty in establishing an unambiguous interrelationship among them; in earlier times matters were even more difficult and we find for example Pearson in the early 20th century speaking of the class Gnetales, rather than the order. G. H. M. Lawrence referred to them as an order, but remarked that the three families were distinct enough to deserve recognition as separate orders. Foster & Gifford accepted this principle, and placed the three orders together in a common class for convenience, which they called Gnetopsida. In general the evolutionary relationships among the seed plants still are unresolved, and the Gnetophyta have played an important role in the formation of phylogenetic hypotheses. Molecular phylogenies of extant gymnosperms have conflicted with morphological characters with regard to whether the gymnosperms as a whole (including gnetophytes) comprise a monophyletic group or a paraphyletic one that gave rise to angiosperms. At issue is whether the Gnetophyta are the sister group of angiosperms, or whether they are sister to, or nested within, other extant gymnosperms. Numerous fossil gymnosperm clades once existed that are morphologically at least as distinctive as the four living gymnosperm groups, such as Bennettitales, Caytonia and the glossopterids. When these gymnosperm fossils are considered, the question of gnetophyte relationships to other seed plants becomes even more complicated. Several hypotheses, illustrated below, have been presented to explain seed plant evolution.
Recent research by Lee EK, Cibrian-Jaramillo A, et al. (2011) suggests that the Gnetophyta are a sister group to the rest of the gymnosperms, contradicting the anthophyte hypothesis, which held that gnetophytes were sister to the flowering plants.
From the early twentieth century, the anthophyte hypothesis was the prevailing explanation for seed plant evolution, based on shared morphological characters between the gnetophytes and angiosperms. In this hypothesis, the gnetophytes, along with the extinct order Bennettitales, are sister to the angiosperms, forming the "anthophytes". Some morphological characters that were suggested to unite the anthophytes include vessels in wood, net-veined leaves (in Gnetum only), lignin chemistry, the layering of cells in the apical meristem, pollen and megaspore features (including thin megaspore wall), short cambial initials, and lignin syringal groups. However, most genetic studies have rejected the anthophyte hypothesis. Several of these studies have suggested that the gnetophytes and angiosperms have independently derived characters, including flower-like reproductive structures and tracheid vessel elements, that appear shared but are actually the result of parallel evolution.
In the gnetifer hypothesis, the gnetophytes are sister to the conifers, and the gymnosperms are a monophyletic group, sister to the angiosperms. The gnetifer hypothesis first emerged formally in the mid-twentieth century, when vessel elements in the gnetophytes were interpreted as being derived from tracheids with circular bordered pits, as in conifers. It did not gain strong support, however, until the emergence of molecular data in the late 1990s. Although the most salient morphological evidence still largely supports the anthophyte hypothesis, there are some more obscure morphological commonalities between the gnetophytes and conifers that lend support to the gnetifer hypothesis. These shared traits include: tracheids with scalariform pits with tori interspersed with annular thickenings, absence of scalariform pitting in primary xylem, scale-like and strap-shaped leaves of Ephedra and Welwitschia; and reduced sporophylls.
angiosperms (flowering plants)
The gnepine hypothesis is a modification of the gnetifer hypothesis, and suggests that the gnetophytes belong within the conifers as a sister group to the Pinaceae. According to this hypothesis, the conifers as currently defined are not a monophyletic group, in contrast with molecular findings that support its monophyly. All existing evidence for this hypothesis comes from molecular studies since 1999. However, the morphological evidence remains difficult to reconcile with the gnepine hypothesis. If the gnetophytes are nested within conifers, they must have lost several shared derived characters of the conifers (or these characters must have evolved in parallel in the other two conifer lineages): narrowly triangular leaves (gnetophytes have diverse leaf shapes), resin canals, a tiered proembryo, and flat woody ovuliferous cone scales. These kinds of major morphological changes are not without precedent in the Pinaceae, however: the Taxaceae, for example, have lost the classical cone of the conifers in favor of a single-terminal ovule surrounded by a fleshy aril.
angiosperms (flowering plants)
Some partitions of the genetic data suggest that the gnetophytes are sister to all of the other extant seed plant groups. However, there is no morphological evidence nor examples from the fossil record to support the gnetophyte-sister hypotheses.
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Coevolution between phytophagous insect antagonists and Carboniferous, Permian, and Triassic seed plant hosts at the level of their respective developmental tool kits with focus on selective forces that drive the logic of transcriptional regulation is proposed in the following essay to explain the origin and evolution of flowering plants and certain Holometabola.
I discuss potential coevolution of insect and seed plant helix-turn-helix proteins, specifically Engraled and Leafy enzymes that bind to cis-regulatory promoters controlling downstream expression of genes determining paedomorphic insect body patterns and plant cone and floral organ development.
The picture of the rock slab on the left is of an indeterminate pentamerous fossil rosid flower (Celastrales, Rosanae) collected by Professor David L. Dilcher from the Lower Cretaceous Dakota Formation of North America. The image was captured in 1981 while the author was visiting Indiana University.
Biologists have been encouraged to think "... both within and outside the paradigm of transcription-encoding factors ..." (page 129, Niklas 2006). The three essays on the succeeding web pages are written from this research perspective.
Were insect and shrub coevolutionary compartments of the late Paleozoic hypoxic icehouse and later hot house, venues of the first angiosperms? Possibly. This question among others is explored in this first of three essays on the origin of angiosperms.
Certain aspects of coevolution of Mesozoic arthropods and seed plants that have a bearing on the origin and diversity of angiosperms are reviewed by Takhtajan (1969), Raven (1977), Thien et al. (1985), Labandeira and Sepkoski (1993), Farrell (1998), Labandeira (1998), Danforth and Ascher (1999), Grimaldi (1999), Wilf et al. (2000), S. Hu et al. (2008), and Labandeira (2014).
Long-branch attraction (LBA) continues to cloud molecular-phylogenetic studies of seed plants, including angiosperms (Lipeng Zeng et al. 2014, Zhenxiang Xi et al. 2014). Sophisticated Bayesian analyses conducted by C. S. P. Foster et al. (2017) report low support (
Do unsolved Ceratophyllales such as extant species of Ceratophyllum represent living descendents of a long branch from the Permo-carboniferous population of Sandrewia texana (Vojnovskyales)?
The diagram on the right is redrawn from Figure 4 on page 341 of D. H. Les (1988), "Hypothetical phylogenetic relationship of Ceratophyllales, Nymphaeales, and modern monocots and dicots." I colorized and changed the font of the typescript to conform to gigantopteroid web page style.
I focus on coevolving, developmentally plastic arthropod and seed plants from the perspective of progenesis as Takhtajan (1976) did in his paper on the origin of angiosperms, but with focus on interacting Paleozoic animal and plant populations. While discussing Armen Takhtajan's premise with Rudolf Schmid, Ph.D., I learned that paedomorphic heterochrony was not under consideration at the time the seminal 1969 book authored by Takhtajan was published.
Proposals considered and discussed below take Armen Takhtajan's hypothesis on a "neotenous origin of flowering plants" (page 209, 1976) one step further.
Specifically, I advance Takhtajan's ideas on angiosperm origins (1969, 1976) from 21st century research perspectives of progenesis melded with rethinking of the paleontology of detached, fossilized remains of underappreciated Paleozoic seed plant organs. Reproductive organs of some lineages of poorly understood Permo-triassic or Permo-carboniferous seed plants were possibly derived from ancestral massive, developmentally plastic, shoot apical meristems (SAMs) yet to be diagnosed from detached and shed foliar organs, seeds, and pollen.
Potential importance of certain Paleozoic seed plant fossils in deciphering the ancestry of flowering plants and paraphyletic clades of gymnosperms reflects my choice of the unusual title for this web site. The best place and time to begin a discussion of the problem is with the biogeography of basal flowering plants and magnoliids.
The Fiji Islands have long been of interest to biogeographers (Raven and Axelrod 1974, Thorne 1986, Morley 2001), to geologists as a tectonic puzzle (Rodda and Kroenke 1984), and to botanists as a "cradle of flowering plants" (title, Chapter 12, Takhtajan 1969), where some "missing links in the chain of angiosperm phylogeny" are known (page 141, Between Assam and Fiji, Takhtajan 1969). Three of the largest islands (Viti Levu, Vanua Levu, and Taveuni) support harmonic "continental" floras (A. C. Smith 1979).
There are several conifers endemic to the Fiji Archipelago including Agathis vitiensis, Acmopyle sahniana, Dacrycarpus imbricatus, Dacrydium nausoriense, Dacrydium nidulum, and Decussocarpus vitiensis. A common gnetophyte (Gnetum gnemon) and a narrowly distributed cycad (Cycas rumphii) occur in the archipelago. Tropical forests of the larger islands yield ten genera of monocotyledonous palms including the monotypic Alsmithia longipes, and the enigmatic magnoliid flowering plant family, Degeneriaceae.
The family Degeneriaceae was discovered in 1942 by I. W. Bailey and A. C. Smith. The only known species at the time, Degeneria vitiensis (pictured below), combines a number of primitive features that have ignited many debates (I. W. Bailey 1949, Cronquist 1968, Takhtajan 1969). A second species of Degeneria has been reported (A. C. Smith 1991).
All total in this rich flora of some 6,000 species, there are 812 endemic angiosperms and conifers, 12 endemic genera, and one endemic flowering plant family (A. C. Smith 1979, 1981, 1991, 1996, Table 1).
The image above is the northwestern face of the Korombasabasaga Range, Viti Levu Island, Fiji as viewed from the road between Namosi and Wainimakutu villages. Distant pinnacles and spires are weathered calc-alkaline Miocene andesites known as the Namosi Volcanics (Rodda and Kroenke 1984).
Despite several decades of effort by morphologists, paleobotanists, and plant biologists, the origin of angiosperms remains enigmatic and mysterious. Some paleontologists regard the problem of flowering plant origins, "... as intractable a mystery today as it was to Darwin 130 years ago" (page 318, Rothwell et al. 2009). Simply put, the origin of angiosperms is a conundrum.
Many bibliographies on angiosperm floral diversity and the origin and evolution of flowering plants are available. Endress (1994, 2001 [a book chapter and two papers], 2004), Bateman et al. (2006), J. A. Doyle (2006), Friis et al. (2006), D. W. Taylor and Hickey (1996 [a book and one paper]), D. E. Soltis et al. (2008), Specht and Bartlett (2009), Dilcher (2010), D. W. Taylor (2010), Friis et al. (2011), J. A. Doyle (2012), and Herendeen et al. (2017) compile particularly relevant reference lists.
Flowering material of Degeneria vitiensis is shown in the right-hand image (photographed by Paddy Ryan, Ph.D.). Fragrance of this species resembles Cananga odorata according to Professor Al Smith (A. C. Smith 1981).
The International Journal of Plant Sciences devotes most of Number 7 of Volume 169 (2008) toward the ongoing search for the earliest flowers, based on an international symposium held during the summer of 2007 at the Swedish Museum of Natural History (von Balthazar et al. 2008). More than twenty articles in Volume 96, Number 1 of the American Journal of Botany explore the origin, evolution, and radiation of flowering plants to celebrate the Charles Darwin Bicentennial (Stockey et al. 2009).
Conrad Labandeira's several reviews on fossil insect-plant phytophagous associations (Labandeira 2000, 2006, 2007 [two papers], 2010, 2014) contain extensive bibliographies. While discussing the effects of ice-house/hot house planetary climatic switches on expansion of land plant invertebrate herbivores Labandeira (2006) states:
"One possibility is that these atmospheric variables have direct physiologic consequences on the selection and turnover of particular plant clades globally, which in turn elicit an associational response from selected clades of insect herbivores."
The preceding statement is quoted from page 425 of C. C. Labandeira (2006), The four phases of plant-arthropod associations in deep time, Geologica Acta 4(4): 409-438.
Some of the historical syntheses include Arber and Parkin (1907), I. W. Bailey (1949), Edgar Anderson (1934), Axelrod (1952, 1970), Leppik (1960, 1968), Raven and Kyhos (1965), Cronquist (1968), Thorne (1968), Melville (1969), Takhtajan (1969, 1976, 1991), Raven and Axelrod (1974), Stebbins (1958, 1974), C. B. Beck (1976), Hughes (1976, 1994), Meeuse (1979), Nair (1979), Krassilov (1977), Retallack and Dilcher (1981 [two papers]), Asama (1982, 1985), Melville (1983), Crane (1985), Meyen (1986, 1988), Dilcher (1986, 2000), J. A. Doyle and Donoghue (1986, 1987), Endress (1987), Friis et al. (1987), Les (1988, 1993), and Les et al. (1991), among others.
Additional compilations on the origin of angiosperms and floral morphology include Krassilov (1991), Thorne (1992), Endress (1993, 2001 [a book chapter and two papers], 2004), Friedman (1992 [two papers]), Stewart and Rothwell (1993), Nixon et al. (1994), Crane et al. (1995), H. D. Zhang (1995), Hickey and D. W. Taylor (1996), D. W. Taylor and Hickey (1992, 1996), Loconte (1996), and Krassilov (1997, 2002), among others.
Crepet (2000), Donoghue and J. A. Doyle (1991, 2000), Frohlich and Parker (2000), Friedman and Floyd (2001), G. Sun et al. (2001), Z.-Y. Wu et al. (2002), Crane et al. (2004), Davies et al. (2004), P. S. Soltis and D. E. Soltis (2004, 2015), Stuessy (2004), D. E. Soltis et al. (2005), De Bodt et al. (2005), J. A. Doyle (1978, 1994, 2005, 2006, 2008, 2012), Friis et al. (2006, 2011), Frohlich (2002, 2003, 2006), and Lipeng Zeng et al. (2014), have contributed to our knowledge of the origin and evolution of flowering plants.
Modern syntheses on the abominable mystery of the origin of angiosperms from unknown Paleozoic seed plant ancestors and modern radiations are published by Frohlich and Chase (2007), Maheshwari (2007), Sokolov and Timonin (2007), Zavada (2007), J. A. Doyle (2008), Endress (2008), D. E. Soltis et al. (2008), Berendse and Scheffer (2009), Friedman (2009), Specht and Bartlett (2009), E. L. Taylor and T. N. Taylor (2009), Xin Wang (2009), Dilcher (2010), Magallón (2010), Stephen A. Smith et al. (2010), Stuessy (2010), D. W. Taylor (2010), Xin Wang (2010), Friis et al. (2011), J. A. Doyle (2012), Amborella Genome Project (2013), Chamala et al. (2013), Seago and Fernando (2013), Crepet (2014), Drew et al. (2014), Goremykin et al. (2015), Simmons and Gatesy (2015), Cascales-Miñana et al. (2016), and Herendeen et al. (2017).
Anthophyte hypothesis. In 1986 James A. Doyle and Michael J. Donoghue proposed that flowering plants were derived from gnetophytes. The anthophyte hypothesis was developed further in later years (J. A. Doyle and Donoghue 1987, Nixon et al. 1994).
After reconsidering incongruent molecular-phylogenetic and morphological data the anthophyte hypothesis was rejected by Donoghue and J. A. Doyle (2000).
"If no living seed plants are closely related to angiosperms the only way to reconstruct the origin of angiosperms is by fitting fossils into the picture, and this can only be done by analysis of morphological characters."
The preceding quote is from page R109 of M. J. Donoghue and J. A. Doyle (2000), Seed plant phylogeny: demise of the anthophyte hypothesis?, Current Biology 10(3): R106-R109.
A reappraisal of the anthophyte hypothesis has been published (Rothwell et al. 2009).
Biome- and paleogeographically-specific hypotheses. Certain ecologists propose that physiological studies of living basal families and species of flowering plants indigenous to island tropical environments may lead to insight on the paleoecology of the angiosperm stem group (Feild et al. 2003, Feild et al. 2004, Feild and Arens 2005, Feild and Arens 2007).
Both an uplands hypothesis (Axelrod 1952) and coastal hypothesis (Retallack and Dilcher 1981) were proposed to explain topographical centers of origin and radiation of the first flowering plants.
Stebbins (1974, 1984) thought that alpine biomes of northern latitudes might have been the center of early radiation of angiosperms. A similar idea, the eastern Asian centers hypothesis, was put forth by G. Sun et al. (2001). Based on the recovery and study of fossil pollen casings (palynomorphs) recovered from deep-sea drill holes, Hochuli and Feist-Burkhardt (2004) suggested that early flowering plants might have evolved in a boreal cradle.
Daniel Axelrod suggested that angiosperms originated in Triassic or Jurassic tropical uplands of Gondwana "... Spreading out into a new adaptive zone, presumably in equable, warm upland areas ..." Axelrod (page 281, 1970) proposed that angiosperms and their insect pollinators dispersed and radiated into semiarid forest openings, and into arid lowlands from tectonic fold belts during the early Cretaceous.
"... we hypothesize that proto-South-East Asia served both as the cradle and centre of diversification of early angiosperms" (page 332, Is the Most Recent Common Ancestor of Angiosperms Now Lost in Proto-southeast Asia Terranes That Are Underwater or Subducted?, Buerki et al. 2014).
Hypotheses suggested by Buerki et al. (2014) contradict classical ideas expressed by Axelrod (1952, 1959) and Krassilov (1997). Dispersal of early angiosperm floras from the tropics poleward was proposed by Axelrod in 1959. A statement quoted from this often overlooked paper is probably pertinent.
"... since angiosperms [Vojnovskyales?] may already have been in existence in upland areas by the Permian [Axelrod 1952], and because the record of the group is exceedingly fragmentary into the Early Cretaceous, the data obviously do not permit us to suggest any one area as the cradle of origin" (page 207, Discussion, Axelrod 1959, the words in [brackets] are mine).
Further, an important study of pollen samples recovered from isolated sedimentary layers in at least one continuous stratigraphic sequence in two deep well cores, reports monosulcate, columellate palynomorphs, and Afropollis, from the Middle Triassic (Anisian) about 240 MYA (Hochuli and Feist-Burkhardt 2013). Definitive paleontological evidence published by Peter Hochuli and Susanne Feist-Burkhardt should be read together with a review of Sanmiguelia paleobiology, also reporting three new localities from the Lower Triassic (Norian) Chinle Formation of southwestern North America (S. Ash and Hasiotis 2013).
Based on Axelrod and Krassilov's cogent arguments, and unequivocal palynological evidence published by Hochuli and Feist-Burkhardt (2004, 2013), the Buerki team (2014) should do more homework and rethink their ideas, in my opinion.
To suggest a specific geographical center of origin of angiosperms, protected place, habitat, or timing from a Gothic or other human perspective ("cradle," "dark,", "dawn," "disturbed," "shady," "stream-like," "wet and wild") might be inconsequential in view of potential >300 million year old divergences of flowering plants from their nearest gymnosperm relatives.
Chloranthoid hypothesis. This hypothesis suggests that flowering plants evolved from chloranthoid ancestors not unlike the modern angiosperm family Chloranthaceae (Leroy 1983).
Arguments presented by Stuessy (2004) in favor of Leroy's proposal include reports of data from molecular systematics that place Hedyosmum (Chloranthaceae, Piperales, Magnoliidae) in a clade basal to other extant angiosperms (Y. L. Qiu et al. 1999).
Developmental and genetic theories. Some of the hypotheses and theories on the origin of angiosperms probably have more to do with the origin of the flower. The two concepts might not be the same (J. A. Doyle 2008).
The main developmentally- and genetically-based hypotheses and theories on the origin of angiosperms and the flower are Asama's Growth Retardation Theory (Asama 1982, 1985), Meyen's gamoheterotophic hypothesis (Meyen 1986, Meyen 1988), Frohlich and Parker's Mostly Male Theory (Frohlich and Parker 2000), Becker and Theißen's out-of-male and out-of-female hypotheses (Becker and Theißen 2003), Baum and Hileman's model of cone and floral development from hermaphroditic strobili (2006), and modifications of the latter two ideas on bisexual strobilus development suggested by Theißen and Melzer (2007) and Melzer et al. (2010).
Another interpretation of the origin of angiosperms from bisexual cone axes, based upon molecular divergence in LEAFY (LFY) genes about 130 MYA, was published by Albert et al. (2002) who link the elimination of one LFY gene paralog "... to the sudden appearance of flowers in the fossil record" (abstract, Albert et al. 2002).
"Our theory may also be tested, without the vagaries of fossil discovery, in modern plants. Of the early-acting genes that control flower development, more should have close homologs (or orthologs, if gene trees are sufficiently resolved to demonstrate orthology) active in male gymnosperm reproductive structures rather than in female structures... In the coming years, topology-violating transformations that are of evolutionary importance may become recognizable using evidence from genes that control development."
The above quotation is from page 167 of M. W. Frohlich and D. S. Parker (2000), The mostly male theory of flower evolutionary origins: from genes to fossils (MMT), Systematic Botany 25(2): 155-170.
Frohlich suggests in several updates of MMT (2001, 2002, 2003) that early Mesozoic Corystospermales might be one of the possible ancestors of flowering plants. Frohlich (2003) placed an interesting idea on the table, namely that potential pollinators of gymnosperms were attracted by ectopic ovules displayed on upper (abaxial) leaf surfaces.
Several elegant studies of LFY gene expression in gymnosperm female cone primordia, using ultrasensitive radioactive probes, clearly demonstrate that transcripts of the gene are present (Shindo et al. 2001, Vásquez-Lobo et al. 2007, Carlsbecker et al. 2013), contradicting the basic premise set forth in MMT. Based on LFY gene expression studies of Gnetum and comparative expressed sequence tag (EST) analyses (Tavares et al. 2010) MMT is yet another unsupported hypothesis on the origin of angiosperms.
Further, the discovery of angiosperm and corystosperm fossils in the same Paleogene flora (McLoughlin et al. 2008) detracts from Frohlich's proposal that corystosperms were flowering plant antecedents.
Studies of wood paedomorphosis may offer new clues on a possible Mesozoic origin of angiosperms (Carlquist 2009), but studies of potentially neotenous gymnosperm secondary xylem development in deep (Paleozoic) time are lacking.
Erbar (2007) summarizes past ideas on a supposed Mesozoic origin of angiosperms from the research perspective of evolutionary-development (evo-devo).
A novel "Mosaic Theory for the Evolution of the Dimorphic Perianth" proposed by Warner et al. (2009) states that:
sepal and petal identities evolved "early in angiosperm history" morphological features of tepals may not have been "fixed to particular organs and were primarily environmentally controlled" later during the evolution of flowering plants "sepalness and petalness became fixed to whole organs in specific whorls, forming distinct sepals and petals, thus removing the need for environmental control in favour of fixed developmental control" reversals observed in certain eudicots (e.g. Berberis [Berberidaceae] and Hypericum [Hypericaceae]) constitute plesiomorphies
Gonophyll theory. Melville develops his earlier ideas on a Gonophyll Theory (1969) in a review published in 1983 that proposes a Permian origin of angiosperms from glossopterids.
Stewart and Rothwell (1993) recapitulated the main steps needed to form the conduplicate carpel using glossopterid-, other seed fern-, and early angiosperm fossils as examples. According to Stewart and Rothwell (1993) these main steps were:
"Grouping of ovules" (fossil evidence: Caytonia, Glossopteris, Petriellaea, and Ottokaria, among others) "Evolution of the fertile axis" (fossil evidence: Caytonia and Petriellaea) "The epiphyllous fertile branch" (fossil evidence: Glossopteris) "Adnation" (fossil evidence: Jambadostrobus and Lidgettonia) "Origin of the bitegmic, anatropous ovule" (fossil evidence: Denkania) "Formation of the carpel" (fossil evidence: Archaeanthus, Lesqueria, among others)
The above bulleted quotes are from pages 461-462 of W. N. Stewart and G. W. Rothwell (1993), Paleobotany and the Evolution of Plants (second edition). Cambridge: Cambridge University Press, 521 pp., with additional comments distilled from E. L. Taylor et al. (2006).
Retallack and Dilcher (1981) presented in-depth discussion of Melville's ideas on a glossopterid ancestry of the angiosperms including a reanalysis of glossopterid fructifications.
Mary White (1986) proposes that glossopterid Microfructi were basal to several parallel but sometimes branching and reticulate lines of evolution leading to the Caytoniales, angiosperms, Cycas (Cycadaceae, Cycadales), Podocarpaceae (Podocarpales), Araucariaceae (Araucariales), and certain catkin-bearing angiosperms including the Casuarinaceae.
Further, White proposed that the glossopterid Megafructi were a second basal group upon which ranalian angiosperms, monocotyledonous flowering plants including Pandanus (Pandanaceae, Pandanales, Arecidae), Williamsonia (a bennettitalean), additional cycads, and certain other angiosperms evolved (M. E. White 1986).
Multiple origins hypotheses. Others suggest that flowering plants evolved from multiple, unrelated seed plant lineages (Edgar Anderson 1934). The polyphyletic-polychromic-polytopic hypothesis (Z.-Y. Wu et al. 2002) and Nair's Triphyletic Theory (Nair 1979) are best placed in this paragraph.
Cyclic angiospermization is reviewed by Krassilov (1997) and Ponomarenko (1998) within the context of a polyphyletic origin of angiosperms. Principal morphologic innovations in angiosperms and gymnosperms according to Krassilov (1997) are:
phyllospermy (growth of ovules on upper or lower leaf surfaces) advent of the micropyle (a suture or opening where pollen tubes penetrate the ovule) pollen (not spore) production taeniae of pollen (elongated pollen grains with parallel ribs) brachyplasty (combination of male and female form) destrobilization (elongation of branching within cones) cupulation (curling of leaves around ovulate clusters)
Paleoherb hypothesis. Flowering plants evolved from herbaceous forms possessing ovule and pollen bearing organs that coalesced over time producing modern flowers according to D. W. Taylor and Hickey (1992, 1996).
Burger published a paper in 1981 suggesting that the earliest angiosperms were monocotyledonous plants. Professor Burger proposed six hypothetical trends in the early evolution of angiosperms:
"Small simple plants preceded large complex plants in the early evolution of angiosperms Scattered vascular bundles within the stem preceded a tubular vasculature with included cylindrical cambium Simple leafy stems without aerial branching preceded complex woody growth with several orders of branching Simple undifferentiated leaves preceded leaves with a clearly differentiated petiole and lamina Leaves with one or a few poorly differentiated orders (ranks) of venation preceded leaves with several clearly differentiated orders of venation A clasping leaf base continuous with the tissue of the stem preceded a leaf base clearly differentiated from the stem; deciduous leaves evolved later and were a major innovation"
The above bulleted quotation is from pages 191-194 of W. C. Burger (1981), Heresy revived: the monocot theory of angiosperm origin, Evolutionary Theory 5: 189-225.
A differing proposal by Dahlgren and Clifford (1982) suggests:
"The ancestors of the monocotyledons were probably shrublets or subshrubs which by environmental conditions (a pronounced alternation between wet and dry periods) evolved compact underground stems, mainly short or long rhizomes from which herbaceous aerial stems were developed ..."
The preceding quotation is from page 344 of R. M. T. Dahlgren and H. T. Clifford (1982), The Monocotyledons: A Comparative Study. New York: Academic Press, 378 pp.
Pseudanthial theory. Eichler (1976) proposed that unisexual gymnosperms may be the ancestors of angiosperms. A discussion of this theory and how it links to the anthophyte hypothesis is presented by T. N. Taylor et al. (pages 877-878, 2009).
Additional discussion is available in several papers that reinvestigate conifer cone abnormalities (Flores-Rentería et al. 2011, Rudall et al. 2011, Carlsbecker et al. 2013).
Seed fern hypotheses. The origin of flowering plants is potentially traceable to Mesozoic seed ferns such as Corystospermales (Frohlich 2002, 2003, 2006) or Paleozoic Glossopteridales (Melville 1969, Retallack and Dilcher 1981, Melville 1983). James A. Doyle suggests that Caytonia (Caytoniaceae, Caytoniales) is a sister group to the angiosperms (J. A. Doyle 1978, 1994, 2006, 2008). Asian botanists postulate that flowering plants evolved from Permo-carboniferous gigantopterids (see G. Sun et al. 2001).
A more intriguing hypothesis was proposed by H. D. Zhang in 1995 (in Chinese). According to a translation provided by Ge Sun et al. (page 162, 2001), H. D. Zhang proposed that gigantopterids evolved into angiosperms in four phases over more than 250 million years of geologic time (note that phrases in parentheses are by Ge Sun et al. 2001, words within brackets  are mine):
(1) Pregnant Stage (as seen in [phyllospermous] Permo-Triassic gigantopterids and sagenopterids (2) Adaptation Stage (folding of leaves into conduplicate carpels [e.g. Sanmiguelia and Schmeissneria] in Triassic-Jurassic anthophytes) (3) Expanding Stage (vicariance of Pangaean seed-plant stock and short- or long distance dispersal from tropical belts to the southern latitudes [and Antarctica]) from Middle Jurassic to Cretaceous time (4) Flourishing Stage (radiation of angiosperms into modern biomes during the Cretaceous to the Neogene Periods)
Zhang's stages are consistent with later ideas developed by Stuessy (2004). Meeuse's Anthocorm Theory (1979) is lodged here.
Unifying theories. Bonafide theories fall into this category despite J. A. Doyle's lukewarm enthusiasm for the Transitional-combinational Theory proposed by Stuessy (2004). Certainly the findings of the Angiosperm Phylogeny Group (APG) have nothing to do with an allopolyploid origin of flowering plants from Late Paleozoic seed plant stock.
Stuessy proposes that carpels evolved first, followed by double fertilization, and then by flowers, slowly over many millions of years, "... perhaps more than 100 million ..." (page 6, Stuessy 2004).
The review by J. A. Doyle (2012) is the latest installment of more than 35 years of research on the origin of angiosperms, which should be read together with a lavishly-illustrated and widely-acclaimed book by Friis et al. (2011).
Apparently, the intent of J. A. Doyle's review of molecular and paleobotanical evidence on the origin of angiosperms was to explore "areas of congruence and conflict and ways in which conflicts might be resolved ..." (page 302, Introduction, J. A. Doyle 2012). Elaborate discussion of 1986 and 1987 milestone syntheses (coauthored with M. J. Donoghue) is incongruent with seed plant organ homologies explained by Mathews and Kramer (2012).
Despite a 2006 discussion of YABBY transcription factors (TFs) and ovule determinants, J. A. Doyle skirts research advances on evo-devo of molecular tool kits, which is a topic of considerable significance toward a deeper understanding of seed plant organ (including cone and floral) homologies based on developmental genetics (Mathews and Kramer 2012).
There is solid biochemical and morphological evidence that flowers are short- (spur-) shoots (Christianson and Jernstedt 2009) whose growth and development is orchestrated by intricate molecular machinery (the tool kit, also coined in the literature as "toolkit") comprised of cis-regulatory modules (CRMs), gene-regulatory networks (GRNs), auxin-based polarity networks (PINs), and cis-acting TFs in germ cells of growing SAMs.
Another review on the origin of flowering plants has surfaced (Cascales-Miñana et al. 2016). In my opinion, this synthesis promised to deliver more than it did.
There are many problems with the dataset used by Cascales-Miñana et al. (2016). Significant discussion of other papers published in the Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences (references listed above) and the Annual Review of Earth and Planetary Sciences (J. A. Doyle 2012, P. M. Barrett 2014), was left-out by the Cascales-Miñana team. Further, much more work is necessary to plot a solution to Darwin's so-called "mystery."
Cascales-Miñana et al. (2016) forgot to review the evolutionary relationships of seed plants with euornithopod transverse grinders and insect mutualists. The team's unusual choice of the Hilton and Bateman 2006 seed plant phylogeny was strange, in my opinion.
Omissions by Cascales-Miñana et al. (2016) of key data-sets published by Misof et al. (2014) and Weishampel and Jianu (2000), cast doubt on outcomes shown in Figure 2.
"What is surprising is the scale of the uncertainty surrounding our basic knowledge of angiosperms. Angiosperm relationships are only now being resolved through the application of various algorithms to the combination of molecular genetics-derived data and morphological data. Yet, the relationship of the angiosperms themselves to nonangiospermous seed plants, or understanding the origin of this major group, still remains a hotly contested mystery ... " (Abstract, Crepet 2014).
Finally, calibrated molecular-phylogenetic analyses by Eguchi and Tamura (2016) and C. S. P. Foster et al. (2017) suggest that Herendeen et al. (2017) should have re-evaluated the morphology and anatomy of Sanmiguelia lewisii before publishing their review in Nature Plants.
Woody magnoliid and ranalian theories and hypotheses. Several theories and hypotheses propose that modern flowering plants evolved from gymnosperms having a bisexual (hermaphroditic) strobilus (page 878, T. N. Taylor et al. 2009).
Arber and Parkin's Strobilus Theory of the Angiosperm Fructification (Arber and Parkin 1907), Delpino's Ranalian Theory (Endress 1993), Braun's Strobilus Theory, Takhtajan's hypothesis on a "neotenous origin of flowering plants" (page 209, 1976), and the woody magnoliid hypothesis may be grouped together for purposes of discussion. Evolution of flowers including carpels, microsporophylls, stamens, and the nested perianth from hermaphroditic gymnosperm strobili is a common thread of these magnoliid-centered proposals.
"From this one may conclude that the angiosperm flower arose most probably from a bisexual entomophilous strobilus, especially as among the earliest gymnosperms examples of bisexuality associated with entomophily are known within the Bennettitales."
The preceding statement is from page 35 of Armen Takhtajan (1969), Flowering Plants: Origin and Dispersal (translated by C. Jeffrey). Edinburgh: Oliver and Boyd, 310 pp.
Woody magnoliid and ranalian theories and hypotheses tie-in with Becker and Theißen's out-of-male and out-of-female hypotheses (Becker and Theißen 2003), Baum and Hileman's model of cone and floral development from hermaphroditic strobili (2006), and modifications of the latter two ideas on bisexual strobilus development suggested by Theißen and Melzer (2007) and Melzer et al. (2010).
Comparing theories and hypotheses. The next section compares some of the theories and hypotheses on the origin of angiosperms and the flower in view of the latest synthesis on the subject by Rothwell et al. (2009). Rothwell et al. (2009) raise several caveats in a critical reevaluation of the three categories of hypotheses and theories on the origin of flowering plants:
One, the anthophyte hypothesis (J. A. Doyle and Donoghue 1986, 1987, Donoghue and J. A. Doyle 2000), "... proposes that the outer seed integument and carpel are derived from fertile structures that already were aggregated into a flower-like reproductive organ (i.e., a strobilus or cone) ..." (page 317, Rothwell et al. 2009).
Two, J. A. Doyle's (1978, 2006, 2008) arguments in favor of the classical caytonialean seed fern hypothesis (Thomas 1925), specifically the glaring absence of transitional fossils and any definable heterochronic lineage linking Caytonia with basal angiosperms, and impossibly complicated evo-devo from deeply conserved cone and floral tool kit perspective, are difficult to accept by some workers. Fossilized material of Caytonia is fragmentary and poorly preserved, leaving interpretation of developmental reproductive structures conjectural (Rothwell et al. 2009).
A third competing set of hypotheses and theories proposes that ovules developed in positions on leaves or stems occupied by pollen-bearing organs.
The MMT (Frohlich and Parker 2000) and Sergei Meyen�s gamoheterotopic hypotheses (1986, 1988) fall into this category according to Rothwell et al. (2009).
I present a brief comparison of some of the hypotheses and theories on the origin of angiosperms in Table 1.
Cells of the table contain one of three responses: "Yes" (colored in yellow), "Congruent" (beige colored), or "No" (uncolored). The second column denotes whether bisexual (hermaphroditic) cone axes consisting of spirally arranged male and female microsporophylls figure prominently in the hypothesis or theory in question. The third column titled "congenital fusion" describes an evolutionary scenario whereby a fertile axis fuses with a subtending leaf sensu Caytoniales (Xin Wang 2010) or Glossopteridales (Melville 1969).
Gene duplications may consist of small gene duplications or WGDs (polyploidy), which are stated by the authors in question as important in the evolution of flowering plants. The term insect mediated is the same as entomophily or may refer to the importance of pollination by insects in the origin of angiosperms.
Data in columns six and seven pertain to explicit evo-devo questions, which have more to do with the origin of the flower rather than the angiosperms as a whole. LEAFY protein gradients might potentially occur in fertile SAMs and cone axes that may affect the downstream expression of homeotic MIKC-type MADS-box genes. Column seven refers to possible interactions between MIKC-type MADS-box B and "C" genes, which are potentially important in the evo-devo of flowers.
The word Permo-triassic in column eight refers to the Permian Period, 251 to 290 MYA, of the Paleozoic Era and/or the Triassic Period, 206 to 251 MYA, of the Mesozoic Era as being the time of origin of angiosperms. A "No" response (the box is uncolored) indicates that the paper or book chapter in question favors a younger Jurassic or Cretaceous origin of flowering plants.
Finally the column labeled "Paraphyly or Polyphyly" denotes whether the scientific paper in question attributes the origin of flowering plants to a natural, intergeneric hybridization event, allopolyploidy, or events that brought together two or more distinct lines of seed plant evolution.