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Origin of Flowering Plants
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E S S A Y C O N T E N T S |
[ The Origin of Angiosperms ]
JOHN M. MILLER, PH.D.
Solving the riddle of the origin of flowering plants might be viewed by some naturalists as the "Holy Grail" of botany. Many books and articles have been written on the subject since the 19th century.
Some of the historical syntheses include Arber and Parkin (1907), Anderson (1934), Axelrod (1952, 1970), Cronquist (1968), Thorne (1968), Takhtajan (1969, 1976, 1991), Raven and Axelrod (1974), Stebbins (1958, 1974), C. B. Beck (1976), Hughes (1976, 1994), Nair (1979), Crane (1985), Meyen (1986, 1988), Dilcher (1986, 2000), and J. A. Doyle and Donoghue (1986, 1987).
Other important compilations on the origin of angiosperms include Friis et al. (1987), Endress (1987, 1993, 2001, 2004), Stewart and Rothwell (1993), Nixon et al. (1994), Crane et al. (1995), Zhang (1995), D. W. Taylor and Hickey (1992, 1996), Krassilov (1977, 1991, 1997, 2002), Crepet (2000), Donoghue and J. A. Doyle (1991, 2000), Frohlich and Parker (2000), G. Sun et al. (2001), Wu et al. (2002), P. M. Soltis and D. E. Soltis (2004), Stuessy (2004), Davies et al. (2004), D. E. Soltis et al. (2005), De Bodt et al. (2005), J. A. Doyle (1978, 1994, 2005, 2006), Friis et al. (2006), and Frohlich (2002, 2003, 2006).
The most recent syntheses on the origin of flowering plants are published by Frohlich and Chase (2007), Maheshwari (2007), Theißen and Melzer (2007), Zavada (2007), and D. E. Soltis et al. (2008).
The picture to the left is a side view of an indeterminate fossil flower unearthed from the North American Lower Cretaceous Dakota Formation. The fossil flower was photographed by the writer in 1981 from Indiana University research and teaching specimens with the permission of Professor David L. Dilcher whose help is greatly acknowledged.
A detached and cut bennettitalean flower as viewed from the side, which is classified as Williamsonia harrisiana appears to the right. It is Figure 10A from Crane (1985), Phylogenetic analysis of seed plants and the origin of angiosperms, Annals of the Missouri Botanical Garden 72: 716-796, reprinted with permission of the Missouri Botanical Garden and Sir Peter Crane.
"Figure 10. Morphology of Bennettitales. -A. Williamsonia harrisiana, longitudinal half-section of 'flower'"
Controversial assertions abound in the scientific literature of the 20th century and several hypotheses and theories exist. None of these ideas when taken as a whole are neither compelling or plausible to many scientists, including the author.
"The flower remains ill-defined and its mode (or modes) of origin remain hotly disputed; some definitions and hypotheses of evolutionary relationships preclude a role for the flower in delimiting the angiosperms" (Bateman et al. 2006)."
The preceding statement is from the abstract on page 3471 of Bateman et al. (2006), Morphological and molecular phylogenetic context of the angiosperms: contrasting the 'top-down' and 'bottom-up' approaches used to infer the likely characteristics of the first flowers, Journal of Experimental Botany 57(13): 3471-3503.
Angiosperms are not the only seed plants that possess flowers or flower-like reproductive structures as the above introductory statements attest. Flowers are found in bennettitaleans and certain gnetophytes such as Welwitschia (Friis et al. 2006).
Many bibliographies on angiosperm floral diversity and the origin of flowering plants are available. Endress (1994, 2004), Bateman et al. (2006), J. A. Doyle (2006), Friis et al. (2006), and D. E. Soltis et al. (2008) compile particularly relevant reference lists.
Douglas E. Soltis et al. (2008) is the most recent paper on the origin of angiosperms.
Labandeira's review (2006) contains the most complete bibliography on fossil insect-plant phytophagous associations. Interestingly, while discussing the effects of ice-house/hot house planetary climatic switches on expansion of land plant invertebrate herbivores Labandeira 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." (Labandeira 2006).
The preceding statement is quoted from page 425 of Labandeira (2006), The four phases of plant-arthropod associations in deep time, Geologica Acta 4(4): 409-438.
Possible Problems with Existing Data Sets:
Some of the past reasoning on the morphologic details and timing of the origin of flowering plants is in doubt and subject to debate. The possible importance of coevolution of phytophagous insect associates and their seed plant hosts might be underplayed in some syntheses on the origin of angiosperms.
Coevolution between phytophagous insect antagonists and Carboniferous, Permian, and Triassic seed plant hosts at the level of their respective developmental tool kits is proposed in the following essay. I reject the widely-held belief of a late Jurassic-early Cretaceous origin of flowering plants.
Interactions between two different, developmentally plastic organisms: invertebrate and plant during many millions of years of late Devonian-early Carboniferous and late Permian global hypoxia might explain the origin of certain insect and seed plant adaptations including small body size and bisexual cone axes.
Tetrapods might have had a surprising effect on the ecology of Mesozoic flowering plants but evidence of coevolution of dinosaurs and early angiosperms is weak (Barrett and Willis 2001). "Tight coevolution" between animal disperser and plant was probably rare (Tiffney 2004).
When more fossil seed plant data become available phylogenetic reconstructions may need to be recomputed to account for errors in phylogenetic inference resulting from long branch attraction (Barrett and Willis 2001). Modified cladistic algorithms are needed to account for possible horizontal transfer of genetic and epigenetic material from epiphytes and symbionts to the stationary plant (Krassilov 2002, Bergthorsson et al. 2004).
Recently reported fossil discoveries of derived, miniature, Amborella-like flowers from the Upper Cretaceous (Krassilov and Golovneva 2004) detract from certain proposals on basal flowering plants and their ecological significance. Preserved invertebrate and plant organs suggest that an already well-developed pollinator-flowering plant mutualism existed in a derived monocot species by the Miocene Epoch of the Paleogene Period (Ramírez et al. 2007).
I do not regard the basal Amborella trichopoda as an "ancestral," "early," or "primitive" flowering plant.
Did a specialized flowering plant and pollinator relationship already exist in the flowering plant family Orchidaceae at the same time that basal Amborella trichopoda (Amborellaceae, Laurales, Magnoliidae) was colonizing the high islands of the southwest Pacific together with the magnoliids classified in Degeneriaceae and Winteraceae?
Painstaking study of Paleozoic gigantopterid and vojnovskyalian reproductive permineralizations is critically needed to determine whether or not these enigmatic Paleozoic seed plants were direct antecedents of flowering plants. This view is consistent with Crepet (2000) who states:
"With both Nymphaea and Amborella at the base of the latest angiosperm tree, a wider range of characters might be expected in archetypical angiosperms or angiosperm sister groups than that implied by previous consensus on Amborella alone. What of complementary projections derived from analysis of seed plant relationships? Do these analyses point toward likely archetypal angiosperms or angiosperm ancestors? No. Not when we incorporate the recent analyses challenging the validity of the anthophytes. Instead, angiosperms become more distantly related to all existing seed plants, leaving a gap populated only by extinct taxa that may or may not be represented in the fossil record" (Crepet 2000).
The above quotation is from Crepet (2000), Progress in understanding angiosperm history, success, and relationships: Darwin's abominably 'perplexing phenomenon, Proceedings of the National Academy of Sciences 97 (24): 12939-12941.
Crepet's realistic commentary quite correctly states that the fossil record of seed plants is extremely fragmentary. For example, almost nothing is known of the reproductive anatomy and morphology of Carboniferous, Permian, and Triassic seed plants.
Carboniferous and Permian gigantopterids and vojnovskyalians may be surprising contributors to the genomes of Triassic "angiosperms" (including Sanmiguelia and bennettitalians).
Existing Theories and Hypotheses:
Loconte (1996) and Frohlich and Chase (2007) review several different hypotheses on the origin of flowering plants. Additional notes appear below:
Pseudanthial theory. Wind pollinated, cone-bearing naked seed plants may be the ancestors of angiosperms according to some. The "pseudanthial theory," of Eichler, Engler, and Wettstein may be placed here (Stuessy 2004). Engler and others concluded that angiosperms evolved from conifers, gnetophytes, and certain catkin-bearing angiosperms such as the forerunners of Casuarina equisetifolia (Casuarinaceae, Casuarinales, Hamamelidae).
Anthophyte Hypothesis. In 1986 Michael J. Donoghue and James A. Doyle proposed that flowering plants were derived from gnetophytes (J. A. Doyle and Donoghue 1986). The anthophyte hypothesis was developed further in later years (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 Donoghue and J. A. Doyle (2000), Seed plant phylogeny: demise of the anthophyte hypothesis?, Current Biology 10(3): R106-R109.
Woody magnoliid theory. Several "theories" proposed that modern flowering plants evolved from Magnolia-like species having strobiloid (cone-like) flowers with many whorled parts not unlike Bennettitaleans. Arber and Parkin's “Euanthial Theory" (Arber and Parkin 1907), Delpino's "Ranalian Theory," Braun's “Strobilus Theory,” and the "Woody Magnoliid Hypothesis" may be grouped together as Stuessy suggests (2004).
Spectacular fossil plant discoveries by Dilcher and Crane (1984) and G. Sun et al. (2001) may require possible refinement of the "Woody Magnoliid Hypothesis."
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).
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 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 Dahlgren and Clifford (1982), The Monocotyledons: A Comparative Study. New York: Academic Press, 378 pp.
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 in a clade basal to other extant angiosperms (Qiu et al. 1999).
Multiple origins hypotheses. Others suggest that flowering plants evolved from multiple, unrelated seed plant lineages (E. Anderson 1934). The “Polyphyletic-Polychromic-Polytopic Hypothesis” (Wu et al. 2002) and Nair's "Triphyletic Theory" (Nair 1979) are best placed in this paragraph. Meeuse's Anthocorm Theory (1979) is lodged here but also discussed above.
Cyclic angiospermization was reviewed in a relatively recent book by Krassilov (1997) who reconsiders traditional ideas of mid-20th century botanists on the origin of flowering plants (Cronquist 1968, Takhtajan 1969) in light of extensive findings of Russian paleoentomologists on pre-anthophyte insect mutualists.
What is angiospermization in the evolutionary-developmental ("evo-devo") context?
If real, how does the mechanism of angiospermization dovetail with developmental recombination and evolution of seed plant characters?
Could angiospermization in a small population of seed plants and resident insect mutualists be triggered by the deleterious effects of temperature swings, global hypoxia, or mass extinction events?
Krassilov (1997) identifies the principal morphologic innovations in seed plants of the angiosperm and gymnosperm grades:
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)
One objective of my review is to define and describe cyclic angiospermization as the process might have happened over geologic time to include a detailed discussion of evidence for angiosperm progenitors, insect mutualists, and flowering plant derivatives.
Gonophyll theory. Ronald Melville was the main proponent of the "Gonophyll Theory" that flowering plants evolved from glossopterids of Mesozoic Gondwana (Melville 1969). Together with voltzialean conifers, gigantopterids and glossopterids are probably the best known fossil seed plant groups of arid, sparsely vegetated Pangaean biomes of the Permian Period. Of the aforementioned plants, at least as presently known, only conifers and some glossopterids persisted beyond the Permo-Triassic Extinction Event, 251 million years ago. The stratigraphic distribution of glossopterids was used in early arguments in support Wegener's Theory of Continental Drift.
In later years, Retallack and Dilcher (1981) presented in-depth discussion on the glossopterid ancestry of the angiosperms. Retallack and Dilcher summarized the morphological diversity of glossopterid fructifications and arranged these graphically to show similarities with flowering plants, in that paper.
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. The following evolutionary plateaus (each advance was determined by the appearance of specific plant genera in the fossil record) in carpel and fruit formation were identified by Stewart and Rothwell (1993):
"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 Stewart and 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).
A nicely illustrated non-cladistic working hypothesis by 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 (a cycadalian seed plant), Podocarpaceae, Araucariaceae (and other southern conifers), and certain catkin-bearing angiosperms including the Casuarinaceae.
White proposed that the glossopterid Megafructi were a second basal group upon which ranalian angiosperms, monocotyledonous flowering plants including Pandanus, Williamsonia (a bennettitalean), additional cycads, and certain other angiosperms evolved (White 1986).
Seed fern hypotheses. Several differing seed fern hypotheses promulgated by American, Asian, and European paleobotanists suggest an origin of flowering plants from Paleozoic and Mesozoic gymnosperm seed fern stock. Research papers that shed light on the origin of flowering plants from pteridosperms include J. A. Doyle (1978, 2006) and Frohlich (2002, 2003).
Doyle and others suggest that the cupule-forming Caytonia or other, as yet unstudied seed ferns were the ancestors of angiosperms (J. A. Doyle 1978, 1994, 2006). However more work is needed to understand the anatomy of ovules and "fruit-bearing" rachises of seed ferns to ascertain homology with functionally equivalent features of the unripened seeds, carpels, and fruits of angiosperms (J. A. Doyle 2006).
The most recent paper on the origin of angiosperms by J. A. Doyle includes new data from recent work on glossopterid reproductive structures. Glossopterids and caytonialians fall into the evolutionary line leading to angiosperms but bennettitaleans and Pentoxylon might also be linked depending on how ovulate and leaf characters are scored (J. A. Doyle 2006).
The relationships of Permo-Carboniferous gigantopterids with evolutionary lines leading to later seed plants, including flowering plants, are at best, conjectural since critical characters of reproductive material remain unstudied. However, leaf venation of gigantopterids is remarkably angiosperm-like. Once defined by study of permineralized reproductive structures, Paleozoic gigantopterids and vojnovskyalians can no longer be ignored in seed plant phylogenetic studies. These points and others are touched on by J. A. Doyle in the latest installment of his work.
However, some workers view the phylogenetic relationships of the Caytoniales, Petriellales, and other seed plants including angiosperms from a different perspective (E. L. Taylor et al. 2006).
Asian botanists have proposed more than once that flowering plants evolved from Permo-Carboniferous gigantopterids (G. Sun et al. 2001). One of the most intriguing hypotheses along the lines of thought expressed earlier by Asama, was developed by Professor Zhang in 1995. According to a translation provided by G. Sun et al. (2001), 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 G. 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). But further refinement of these interesting proposals will require solid paleontologic data drawn from painstaking study of as yet discovered permineralizations of extinct gigantopterids sensu lato.
Biome- and paleogeographically-specific hypotheses. Interestingly 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."
In a later review of early angiosperm history based upon new evidence having a bearing on the antiquity, center of origin, and evolution of flowering plants, Axelrod proposed that angiosperms originated in Triassic-Jurassic tropical uplands of Gondwana. "Spreading out into a new adaptive zone, presumably in equable, warm upland areas," Axelrod proposed that angiosperms and their insect pollinators dispersed and radiated into semiarid forest openings, and into arid lowlands from Cretaceous geologic fold belts during the Early Cretaceous (Axelrod 1970).
To suggest a specific geographical center of origin, protected place, or habitat from the Gothic human perspective ("cradle", "shady," "stream-like," "dark," "disturbed, "wet and wild") might be inconsequential.
Feild et al. (2004) base their conclusive ideas on early angiosperm ecology from the phylogenetically robust ANITA clade. However, despite possibly wide agreement among certain workers that Amborellaceae and Hydatellaceae are basal angiosperms (D. E. Soltis and P. S. Soltis 2004, Rudall et al. 2007); Amborella trichopoda is almost certainly not an early flowering plant.
Developmentally and genetically-based theories. Ideas on the origin of angiosperms based on evidence from the study of ontogeny of seed plants include Asama's Growth Retardation Theory (Asama 1960, 1982), Meyen's Gamoheterotophic Hypothesis (Meyen 1986, Meyen 1988), Frohlich and Parker's Mostly-male Theory (Frohlich and Parker 2000), and Becker and Theißen's Out-of-male and Out-of-female hypotheses. The Out-of-male and Out-of-female hypotheses are based on a floral homeotic protein quartet model and evolutionary-development (evo-devo) of pollen-bearing and ovular organs of cone axes (Becker and Theißen 2003, Theißen and Melzer 2007).
"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 Frohlich and Parker (2000), The mostly male theory of flower evolutionary origins: from genes to fossils (MMT), Systematic Botany 25(2): 155-170.
Frohlich suggests in two updates of MMT (2002, 2003) that early Mesozoic Corystospermales might be one of the possible ancestors of flowering plants. Frohlich (2003) offered the interesting idea that potential pollinators of gymnosperms were attracted by ectopic ovules displayed on upper (abaxial) leaf surfaces. However, the discovery of Paleogene angiosperm and corystosperm fossils in the same fossiliferous beds on the island of Tasmania (McLoughlin et al. 2008) detracts from Frohlich's proposal that corystosperms were flowering plant antecedents.
A paper on the origin of angiosperms (De Bodt et al. 2005) proposes that ancient polyploids provided genetic material (gene duplications) needed for flowering plant evolution. De Bodt et al. conclude:
"Given that such genes [developmental, regulatory, and signaling genes] are considered important for introducing phenotypic variation and increase in biological complexity, linking ancient polyploidy events with decisive moments in evolution becomes less speculative and the origin and evolution of angiosperms perhaps less of a mystery."
The above quotation is from page 596 of De Bodt et al. (2005), Genome duplication and the origin of angiosperms, Trends in Ecology and Evolution 20(11): 591-597. The phrase in brackets [] is mine.
Unifying theories. Bonafide theories fall into this category. Stuessy's Transitional-combinational Theory which draws on information from several scientific disciplines, is the most up-to-date theory in this category (Stuessy 2004). 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."
Comparing Theories and Hypotheses:
The next section compares some of the theories and hypotheses on the origin of angiosperms (Table 1). Frohlich and Chase (2007) provide the reader with a nice comparison of theories and hypotheses on the origin of flowering plants.
A few elements of Asama's Growth Retardation Theory (Asama 1960, 1982), Meyen's Gamoheterotophic Hypothesis (Meyen 1986, Meyen 1988), Frohlich and Parker's Mostly-male Theory (Frohlich and Parker 2000), and Becker and Theißen's Out-of-male and Out-of-female hypotheses (Becker and Theißen 2003, Theißen and Melzer 2007) dovetail with- and potentially support a thigmomorphogenetic/coevolutionary hypothesis on the origin of flowering plants.
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Table 1. Preliminary Comparison of Hypotheses and Theories on the Origin of Angiosperms
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Proposal |
Ontogenetic Component? |
Monopodial Growth? |
Insect-Mediated? |
Permo-Triassic Origin? |
Cyclic from Parallel Lineages? |
Shrub/Tree Architecture? |
Anthocorm Theory |
No |
Yes |
Possibly |
No |
Possibly |
Possibly |
Anthophyte Hypothesis |
No |
Yes |
No |
No |
No |
Yes |
Athcorn Theory |
No |
Possibly |
No |
No |
No |
Possibly |
Chloranthoid Hypothesis |
No |
Possibly |
Possibly |
No |
No |
Yes |
Euanthial Theory |
No |
Yes |
Possibly |
No |
No |
Yes |
Gamoheterotopic Hypothesis |
Possibly |
Possibly |
No |
No |
Possibly |
Possibly |
Gonophyll Theory |
No |
Possibly |
Possibly |
Yes |
Possibly |
Yes |
Growth Retardation Theory |
Possibly |
Possibly |
No |
Yes |
No |
Possibly |
Monocot Hypothesis |
No |
Possibly |
No |
No |
Possibly |
Possibly |
Mostly-Male Theory |
Yes |
Possibly |
No |
No |
No |
Possibly |
Multiple Origins Hypotheses |
Possibly |
Possibly |
Yes |
Yes |
Yes |
Yes |
Paleoherb Hypothesis |
Possibly |
Possibly |
No |
No |
No |
No |
Polyphyletic-Chromic-Topic Hypothesis |
Possibly |
Possibly |
Possibly |
No |
Yes |
Possibly |
Pseudanthial Theory |
No |
Possibly |
No |
No |
No |
Yes |
Ranalian Theory |
No |
Yes |
No |
No |
No |
Yes |
Seed Fern Hypothesis |
Possibly |
Possibly |
No |
No |
Possibly |
Yes |
Strobilus Theory |
No |
Yes |
Possibly |
No |
Yes |
Yes |
Transitional-Combinational Theory |
Possibly |
Possibly |
Yes |
Yes |
Yes |
Possibly |
Triphyletic Theory |
No |
Possibly |
Possibly |
Yes |
Yes |
Possibly |
Woody Magnoliid Hypothesis |
No |
Possibly |
No |
No |
No |
Yes |
First Clues on the Origin of Angiosperms:
Having compared and discussed some of the previous hypotheses on the origin of flowering plants this chapter outlines some of the biodiversity of extinct forms that might offer some clues on solving the riddle of angiosperm beginnings.
The picture of the rock slab to the left is of an indeterminate pentamerous fossil flower (Celastrales, Rosidae) 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.
The first clue that sheds light on the shadowy origin of flowering plants comes surprisingly from study by oil and gas explorers and geochemists of fossilized biomarkers and molecular traces which are recoverable from mud logs of well boreholes.
Molecular tracers include diagenically altered, naturally occurring but fossilized triterpenoids known as oleanone triterpanes (oleananes). Oleananes occur in fossilized leaf material of certain gigantopterids, bennettitaleans, and flowering plants, but are absent from samples of several other fossil seed plants (D. W. Taylor et al. 2006).
Oleanone triterpanes are routinely used by oil and gas drillers to locate fossiliferous terrestrial and shallow (possibly deltaic) marine deposits, with an identifiable higher plant input.
Mud-loggers are able to ascertain higher plant input into a core segment of a stratigraphic horizon pulled-up from the well well-site gas chromatography and mass spectrometry, and microscopic analysis of animal and plant microfossils including pollen and vascular plant fragments in core samples.
Are oleonone triterpanes diagenetic products of phytoecdysones and terpenes including iridoids produced by phytophagous insect associates of gigantopterids, bennettitaleans, and angiosperm eudicots?
The image to the right is a piece of rock slab containing the largest known gigantopterid fossil leaf compression collected by the author and colleagues. It has been described as Delnortea abbottiae (Gigantopteridaceae, Gigantopteridales), Lower Permian (Leonardian) Road Canyon Formation of the Del Norte Mountains of southwestern North America (photographed by writer on the day the fossil was discovered in 1982).
Based upon study of leaf and midrib permineralizations Mamay et al. (1988) suggested that certain gigantopteroids may be antecedents of- or share commonality with Gnetum. With the notable exception of D. W. Taylor et al. (2006), most of the phylogenetic reconstructions and essays on the origin of flowering plants either do not include gigantopterids (Mathews and Donoghue 1999, Qiu et al. 1999, Soltis et al. 2005), or only briefly mention them as a possible group for study (J. A. Doyle 2006).
Why do certain workers ignore oleanane-containing gigantopterids as possible ancestors or relatives of flowering plants and bennettitalians? It is just that paleobotanists have only just begun to find and describe permineralizations of these enigmatic seed plants.
None of the work on Permian gigantopterids published to date convincingly demonstrates physical connections between reproductive structures, stems, roots, and leaves. Whole plant morphologies are completely unknown for this group of Paleozoic seed plants.
Permo-Carboniferous gigantopterids may be surprising contributors to the genomes of Triassic seed plants including angiosperms and bennettitaleans.
Characters of Angiospermous Seed Plants:
Classic books on the origin of angiosperms (Cronquist 1968, Takhtajan 1969) outline the salient differences between the vegetative anatomy of angiosperms and gymnosperms. These are reviewed in greater detail in the many textbooks on plant morphology and paleobotany. Some of the main, traditional defining vegetative characters (though not exclusive) include:
leaves with complex venation, often meshed and areolate (but also known in gigantopterids, gnetophytes, and nilssonialeans, among others)
waxy leaf cuticles
biosynthetically and evolutionarily derived defense substances (alkaloids, polyacetylenes, steroids, and terpenoids); and antioxidants and ultraviolet radiation shielding molecules (flavonoids)
oleanone triterpanes (oleananes derived from diagenically altered terpenoids)
abscission layer in petioles (known in the gigantopterids Delnortea and Vasovinea)
sieve tube complexes consisting of companion cells and sieve tube elements
libriform fibers of the phloem (known in the gigantopterids Delnortea and Vasovinea, among others)
vessels in wood (vessels are also found in gigantopterids, gnetophytes, pteridophytes [ferns] and sphenopsids [horsetails] but absent in some flowering plant orders)
bifacial cambium (known in the gigantopterids Delnortea and Vasovinea, among others)
multilacunar nodes
few seed leaves (Degeneria has many [four or more] cotyledons)
Some definitive reproductive characters of flowering plants (with some exceptions noted in parentheses) include:
production of flowers (bennettitaleans possess flower-like strobili)
ovules enclosed within carpels to form seeds and fruits
ovules with more than one protective layer of cells termed integuments (however, some flowering plants have only a single layer; conifers such as Taxus and Gnetum possess two layers)
tiny female gametophytes to form embryo sacs (but also known in gnetalians)
micropylar region of ovules lacking pollen chambers and pollination droplets
double fertilization (absent in some flowering plants, present in certain gnetophytes e.g. Ephedra)
stamens and not microsporophylls (Degeneria has microsporophylls in place of stamens)
pollen with a perforate-reticulate tectum and/or columellate inner wall
pollen with few internal cells (essentially a miniature male gametophyte that develops inside of a spore)
What are the seed plant groups upon which to base a study of the origin and evolution of early angiosperms and the derived crown group? When in geologic time do we begin this study? Table 2 outlines the fossil history of the main taxonomic orders of seed plants.
Each cell in the table below lists the number of known fossil genera for the taxonomic order named at the beginning of each row. For example, the Order Glossopteridales consists of the single whole plant genus Glossopteris which is denoted by a "1" in the cell. The integer in parentheses (9), denotes the approximate number of morphotype genera belonging to Glossopteris. The fossil history and nomenclature of gymnosperms is sufficiently complex and humbling to warrant a cautious approach.
It was impractical to include the more than 78 orders of flowering plants in this table, the bulk of which did not appear in the fossil record until the Paleogene.
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Table 2. Fossil History of the Provisional Orders of Seed Plants (Excluding Flowering Plants).
|
Order |
Devonian |
Carboniferous |
Permian |
Triassic |
Jurassic |
Cretaceous |
Paleogene |
Bennettitales |
0 |
0 |
0 |
6(8) |
6(8) |
6(8) |
0 |
Callistophytales |
0 |
3(12) |
2(2?) |
0 |
0 |
0 |
0 |
Caytoniales |
0 |
0 |
0 |
1(?) |
3(4) |
3(4) |
0 |
Coniferales |
0 |
0 |
0 |
9(11) |
9(11) |
46 |
46 |
Cordaitales |
0 |
2(9) |
2(9) |
0 |
0 |
0 |
0 |
Corystospermales |
0 |
0 |
1(1) |
3(16) |
3(16) |
3(16) |
1(1) |
Cycadales |
0 |
0 |
2 |
3 |
1(3) |
1(3) |
10 |
Czekanowskiales |
0 |
0 |
0 |
1 |
5 |
5 |
0 |
Gigantopteridales |
0 |
1(?) |
7(10) |
1(?) |
0 |
0 |
0 |
Ginkgoales |
0 |
0 |
0 |
8(3) |
8(3) |
8(3) |
1 |
Glossopteridales |
0 |
0 |
1(9) |
1(9) |
1? |
0 |
0 |
Gnetales |
0 |
0 |
1 |
6 |
6 |
6 |
3 |
Hydrospermales |
4(6) |
0 |
0 |
0 |
0 |
0 |
0 |
Lagenostomales |
1(14) |
1(14) |
1(14) |
0 |
0 |
0 |
0 |
Nilssoniales |
0 |
0 |
0 |
2 |
2 |
0 |
0 |
Peltaspermales |
0 |
0 |
3(16) |
3(16) |
0 |
0 |
0 |
Pentoxylales |
0 |
0 |
0 |
0 |
1 |
1(?) |
0 |
Petriellales |
0 |
0 |
0 |
1 |
0 |
0 |
0 |
Taxales |
0 |
0 |
0 |
0 |
1 |
1(3) |
6(3) |
Trigonocarpales |
4(22) |
4(22) |
4(22) |
0 |
0 |
0 |
0 |
Vojnovskyales |
0 |
1(1) |
3 |
0 |
0 |
0 |
0 |
Voltziales |
0 |
1(8) |
1(8) |
1(8) |
1(8) |
0 |
0 |
Examination of the table above reveals at least two evolutionary trends among Paleozoic gymnosperms: the Gigantopteridales which possess morphological features similar to the Bennettitales and Nilssoniales, "die-back" at the Permo-Triassic boundary, coincident with the greatest extinction level event of all time. Did the surviving populations of gigantopterids evolve into bennettitalean genera such as Williamsonia and Vardekloeftia?
The simplistic presentation in Table 2 offers an important clue on evolution and diversification of the Bennettitales, Caytoniales, Corystospermales, Czekanowskiales, Gigantopteridales, Glossopteridales, Nilssoniales, Peltaspermales, Pentoxylales, and Petriellales. These seed plant groups "disappear" from the fossil record just a few million years before the first flowering plant orders "appear." Is this a coincidence? Probably not. Are we focusing in the right place and time to solve the riddle?
The next section of the essay is a discussion of cladogenesis of flowering plants from major groups of extinct seed plants.
Cladogenesis of Seed Plants:
In 1985 Sir Peter Crane compiled detailed lists of characters of the seed plant orders known and cast these in a cladistic framework with a discussion of character polarity and homology, stratigraphic history, and evolutionary relationships. The original article by Crane (1985) and later paper (Crane et al. 2004) complement J. A. Doyle's (2006) attempts to reconstruct the evolutionary history of seed ferns and basal angiosperms.
The image to the right is a rock slab containing a compression of Cordaitanthus (Cordaitaceae, Cordaitales) from Carboniferous rocks of eastern North America. I thank Professor David L. Dilcher for giving me permission to photograph this specimen from the paleobotanical collection of Indiana University in 1981.
By following the underlined hot links in the bulleted list below the reader may navigate to another essay and find a detailed discussion of the taxonomic group in question. The major taxonomic orders of seed plants (except flowering plants) include:
Bennettitales
Callistophytales
Caytoniales
Coniferales
Cordaitales
Corystospermales
Cycadales
Czekanowskiales
Gigantopteridales
Ginkgoales
Glossopteridales
Gnetales
Hydrospermales
Lagenostomales
Nilssoniales
Peltaspermales
Pentoxylales
Petriellales
Taxales
Trigonocarpales
Vojnovskyales
Voltziales
Phylogenetic framework. The most recent paper on the origin of angiosperms (D. E. Soltis et al. 2008) outlines progress on the use of phylogenetics to resolve the "big picture," of seed plant evolution. Figure 1 on page 5 of D. E. Soltis et al. (2008) is a place to begin discussion of cladogenesis of flowering plants. Additional details on the pros and cons of cladistic methodologies in estimating stem and crown group angiosperms appear in Bateman et al. (2006), among others.
Caytonia is a sister group to angiosperms in many emerging phylogenetic reconstructions (D. E. Soltis et al. 2005), however two critical seed plant groups, gigantopterids and Vojnovskyales are omitted from most data sets with the notable exception of D. W. Taylor et al. (2006). Corystospermales thought by some workers as possible angiosperm antecedents (Frohlich 2002) are not sister to the branch leading to flowering plants, but cluster instead in another clade with peltasperms, Gnetales, conifers, and Ginkgo (D. E. Soltis et al. 2008).
Based on molecular phylogenetic studies, a close relationship of conifers with Gnetales is supported (Y.-L. Qiu et al. 1999, Magallón and Sanderson 2002, Burleigh and Mathews 2004). Based on the findings of Qiu et al. (1999) and others, the anthophyte hypothesis was rejected by Donoghue and J. A. Doyle (2000).
Amborellales, Nymphaeales, and Austrobaileyales are now widely regarded as basal to most of the living families and orders of flowering plants (Mathews and Donoghue 1999, Y.-L. Qiu et al. 1999, Y.-L. Qiu et al. 2000, Wikström et al. 2001, Zanis et al. 2003, Leebens-Mack et al. 2005, Y.-L. Qiu et al. 2005, and D. E. Soltis et al. 2005, among others).
"It seems the perpetuation of the 'abominable mystery' is due more to a disagreement over the cladistic position of various fossil taxa in relationship to the angiosperm crown group, than the lack of data."
The preceding quotation is from page 127 of Zavada (2007), The identification of fossil angiosperm pollen and its bearing on the time and place of the origin of angiosperms, Plant Systematics and Evolution 263: 117-134.
Key phylogenetic reconstructions of angiosperms published in the scientific literature of the last decade include Goremykin et al. (1997), Kuzoff et al. (1998), Nandi et al. (1998), Hilu et al. (2003), Crepet et al. (2004), J. A. Doyle (2001, 2006), Magallón and Sanderson (2005), and D. W. Taylor et al. (2006).
Many other workers infer phylogeny of angiosperms from cladistic analysis of nucleic acid and protein sequences, or a combination of biochemical, genetic, and morphological data (Magallón et al. 1999, Barkman et al. 2000, Bowe et al. 2000, Mathews and Donoghue 2000, Sanderson and J. A. Doyle 2001, Chaw et al. 2004, Janssen and Bremer 2004, Sanderson et al. 2004, Y.-L. Qiu et al. 2006, among others).
David W. Taylor et al. (2006) publish one of the few accounts of seed plant phylogeny that includes gigantopterids, a group of gymnosperms incertae cedis with possible close ties to both flowering plants and Bennettitales. The phylogram below is redrawn from Figure 2 of D. W. Taylor et al. (2006). Bootstrap confidence limits are left off the graphic. Enigmatic Vojnovskyales are omitted by D. W. Taylor et al. (2006), despite possible evolutionary ties with Sanmiguelia (Crane 1985, page 779), a monocot-like Triassic fossil (Cornet 1989).
Several taxa depicted in the phylogeny of seed plants redrawn below may be unfamiliar to the reader. The Elkinsiales is a group of early seed ferns (Serbet and Rothwell 1992). Lyginopteris is classified in the order Lyginopteridales. Quaestora and Medullosa are other early Paleozoic seed fern genera.
Groups traditionally classified by Cronquist (1981) as angiosperms are shown in red-type on the diagram. Cycads and ginkgos are displayed as green letters. Gigantopterids are labeled in orange. Corystosperms and glossopterids are denoted by blue type. Common groups of conifers appear in brown type while seed ferns are shown in indigo brown type.
The preceding cladogram is redrawn from Figure 2 on page 187 of D. W. Taylor et al. (2006), Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils, Paleobiology 32(2): 179-190.
"...one of the biggest remaining challenges facing evolutionary biologists is ascertaining the fossil lineages that represent the closest relatives of angiosperms."
The preceding phrase is from page 4 of D. E. Soltis et al. (2008), Origin and early evolution of angiosperms, Pp. 3-25 In: C. D. Schlichting and T. A. Mousseau (eds.), Annals of the New York Academy of Sciences, Volume 1133 Issue, The Year in Evolutionary Biology 2008. New York: The New York Academy of Sciences, 203 pp.
What is the age of the flowering plant clade based upon molecular evidence? Bell and colleagues (2005) present an overview of the many attempts underway to date the time of first divergence of angiosperms. An analysis of the data using the penalized-likelihood (PL) cladistic method estimates the age of angiosperms at 251.77 million years ago (Schneider et al. (2004). Based upon Bayesian "relaxed-clock" methods (Thorne and Kishino 2002), Bell et al. (2005) age the crown group of angiosperms from 106.1 to 229.4 M.Y.A.
Is it merely coincidental that the age determined by penalized-likelihood methodology is the same as the estimated time of the end-Permian extinction (EPE)? Should the evolutionary clock and root of the seed plant clade that leads to flowering plants be calibrated to the time of the end-Permian extinction, 251.3 million years ago?
Should molecular systematists analyze characters of plant and insect developmental tool kits to better understand possible co-cladogenesis before drawing conclusions on the origin of flowering plants and phytophagous insect associates?
Cladogenesis of Insects Living in Association with Plants:
Entomologists have made progress on understanding phylogenetic relationships of the major groups of insects (Wootton 1981, Lawrence and Newton 1982, Wilf et al. 2000, Labandeira 2002, Grimaldi and Engel 2005, Labandeira 2006, Lopez-Vaamonde et al. 2006, Moreau et al. 2006, Gómez-Zurita et al. 2007, Hunt et al. 2007, Gómez-Zurita et al. 2008).
It is of interest to students of insect evolution that the Holometabola probably evolved from hemimetabolous ancestors during the Carboniferous ice-house (Grimaldi and Engel 2005), about the same time that oxygen levels in Earth's atmosphere reached a low of 13% (Berner and Kothavala 2001, Ward et al. 2006, Labandeira 2006). Grimaldi and Engel (2005, page 333) raise the key question, "how did they [Holometabola] evolve?
Did the evolution of holometabolus insects from hemimetabolous ancestors occur as a result of developing global hypoxia as a selective force during the late Devonian-early Carboniferous ice-house and following the end-Guadalupian extinction of the late Permian Period? Can we link cladogenesis of the Holometabola to molecular evolution of gas-binding hemocyanin and hexamerin moulting storage enzymes?
The first of the hexamerin molecular evolutionary radiations corresponds with the late Devonian/early Carboniferous hypoxic ice-house Earth from 360 to 320 M.Y.A. (Hagner-Holler et al. 2007), and the initiation of Insect Herbivore Expansion Phase 2 (Labandeira 2006). During the late Devonian-early Carboniferous ice-house, hypoxic interval seven clades of hexamerin storage proteins diverge from primitive Plecoptera (stoneflies) leading to many derived hemimetabolous and holometabolous insect orders (Hagner-Holler et al. 2007).
Molecular approaches employing DNA and ribosomal RNA are providing valuable insight into the cladogenesis of ants, bees, and leaf beetles (Gómez-Zurita and Galián 2005, Brady et al. 2006, Danforth et al. 2006, J. Hughes et al. 2006, Moreau et al. 2006, Gómez-Zurita et al. 2007, Hunt et al. 2007, Gómez-Zurita et al. 2008, Hunt and Vogler 2008).
It is widely accepted that certain phytophagous insect groups diversified together with their flowering plants hosts (Wilf et al. 2000, Labandeira 2002). However, molecular phylogenies of chrysomelid leaf beetles suggests a younger age of the group than previously realized (Gómez-Zurita and Galián 2005, Gómez-Zurita et al. 2007).
What are the known feeding groups of ancient insects deduced from studies of plant fossils and permineralized insect guts? Labandeira (1998, 2006) identified several functional feeding groups of invertebrates in his two review papers on the subject:
External foliage feeders
Piercers and suckers
Borers
Galling insects
Leaf miners
Sporiovores
Pollenivores
Surface fluid feeders
Can systematic biologists and ecologists find traces of the phylogenetic signal left behind by the original inhabitants of Permo-Triassic "shrub lifeboats" through study of phytophagous associates of extant seed plants?
Assuming coevolution of phytophagous Coleopterans with angiosperms, various proposals on rapid diversification of flowering plants during the Albian Age of the Gallic Epoch of the early Cretaceous Period (Friis et al. 2006) are inconsistent with molecular-based phylogenies of Coleoptera that suggest a Triassic origin of certain non-chrysomelid beetle lineages (Hunt et al. 2007).
With possible insect and seed plant co-cladogenesis in mind, I now present a thigmomorphogenetic/coevolutionary hypothesis on the origins of flowering plants:
[ Thigmomorphogenetic/Coevolutionary Hypothesis ]
During the hypoxic late Devonian-early Carboniferous ice-house (DeCARB), invertebrate hemocyanin respiratory enzymes and hexamerin food storage and moulting proteins of plecopteran (stonefly) ancestors diverged, leading to novel multimeric proteins in several hemimetabolous and holometabolous clades of modern insects. At the same time, key vascular plant developmental genes and their dimeric and multimeric transcription factors including Class III HD-Zip, APETALA, AP2, ARF, DELLA, MIKC Type 2 MADS-box, PIN, GRAS, KNOX, LEAFY, YABBY, and TIR, were evolving into molecular novelties of diverging seed plant lineages.
Coevolution between insect antagonist and seed plant host developmental tool kits might have occurred during the DeCARB at the molecular level with local hypoxia and cold temperature as underlying and potentially powerful selective forces.
Global oxygen levels declined to 13% during the course of millions of years of the DeCARB. Resident chewing, crawling, ovipositing, piercing, and sucking insects probably became dependent on host seed plant shrubs and trees for food, oxygen gas; and shelter from predators, cold temperatures, and ultraviolet radiation. Phytophagous insect associates of Permo-Carboniferous vegetation potentially coevolved with their oxygen-generating plant hosts.
The end-Guadalupian carbon cycle event (GuCCE) and associated global hypercapnia reinforced the already close association between Permian plants and protocoleopterans, weevils, and other hemi- and holometabolous insects, ostensibly established after the DeCARB. Resident phytophagous insect associates of developmentally plastic Permian seed plant shrubs including gigantopterids and vojnovskyalians, allowed stressed hemimetabolous insect mutualists to survive hot, hypoxic environments.
Permo-Triassic seed plants were probably confined to small isolated populations indigenous to fragmented biomes and fitness landscapes resulting from the deleterious effects of the end-Permian extinction (EPE). Surviving insects of the EPE and Triassic-Jurassic boundary carbon cycle event (TrCCE) fed, reproduced, and might have secreted biologically active molecules while trampling the surfaces of shoot apical meristems (SAMs) and accessory fertile cone axes.
Signaling molecules such as jasmonates and volicitins originating in the bodies of phytophagous insect associates of Permo-Triassic shrubs and trees, when applied to growing points of the host plant with mechanical force might have affected biosynthesis of certain phytohormones including gibberellic acid (GA). Transduction of biologically active insect signaling molecules potentially stimulated biosynthesis of GA, activating, modifying, and upregulating homeotic selector and meristem identity genes affecting developmental switches in expanding bisexual cone axes.
Phytoecdysones originating in tissues of Carboniferous and Permian seed plants could have signalled the hemocyanin respiratory and hexamerin storage protein manufacturing machinery of eggs and instars of phytophagous insect antagonists profoundly affecting their development and body size.
Permo-Triassic shrubs and trees ostensibly developed anatomical and biochemical defenses against both invertebrate and vertebrate herbivores possibly ameliorating mechanical damage to SAMs and accessory fertile meristems. Dependence of insect colonies on seed plant shrubs and trees might have been reinforced by paleoclimatic changes triggered by global catastrophe.
Sexual reproductive traits of certain developmentally plastic Paleozoic seed plants including early Mesozoic flowering plants are ostensibly intertwined with 200 to 300 million year-old gene duplications and subsequent evolution of protein dimers and tetramers essential to meristem, organ, and reproductive module identity.
At the same time that gene duplications led to the evolution of floral dimers and quartets in Paleozoic shrub lifeboats, certain phytophagous insect associates underwent a second burst of molecular evolution of hexamerin storage proteins. Molecular evolution comprising the second burst of hexamerin diversification led to Coleoptera (bees), Diptera (flies), Hymenoptera (bees and wasps), and certain Lepidoptera (moths).
Moulting in developmentally plastic insect mutualists of Permian seed plant shrub- and tree-like lifeboats was probably affected by phytoecdysone hormones manufactured by the host seed plant. Signaling of respiratory protein genes of the insect genome by the plant, and mechanical and secretory activities of insect antagonists leading to signaling of host plant homeotic genes in SAMs, were likely hallmarks of Permo-Carboniferous and Permo-Triassic coevolutionary compartments.
Enveloped and surrounded by an acidified hypoxic desert, shrub lifeboats were venues where reciprocal, simultaneous, and specialized communication between invertebrate and plant took place at the molecular level. Insect hexamerins might have been hypoxia-inducible moulting storage proteins of the developmental tool kit of the larger-bodied insects of Carboniferous and Permian time. Insect bodies became smaller in plant-dwelling populations that survived the EPE and TrCCE.
Innovative traits of Permo-Triassic seed plants possibly included double fertilization, encapsulation of female gametophytes inside hardened ovules, folding of megasporophylls into carpels, and development of staminodes and stamens from laminar microsporophylls, but critical fossil evidence is needed. Populations of Permo-Triassic seed plants were ostensibly subjected to the vagaries of genetic drift, gene flow, meiotic drive, mutation, and natural selection of phenotypes resulting from developmental recombination, genetic accommodation, and gene duplications potentially leading to evolutionary change and possible angiospermization.
Paleozoic gigantopterids, glossopterids, and vojnovskyalians may be surprising contributors to the genomes of Triassic seed plants including angiosperms, bennettitalians, corystosperms, and pentoxylalians.
Selection pressures in populations of Carboniferous and Permo-Triassic seed plant populations were probably much greater than believed. An herbaceous origin of flowering plants cannot be explained by mutualism and coevolution of insects and seed-bearing shrub hosts alone. A Late Jurassic aquatic origin for flowering plants is incongruent with likely deleterious effects of sulfuric acid poisoning of lakes, shorelines, and wetlands, caused by basalt outpouring from the Central Atlantic Magmatic Province (CAMP), which is associated with the Triassic-Jurassic boundary carbon cycle event (TrCCE).
Assuming coevolution of phytophagous Coleopterans with angiosperms, various proposals on rapid diversification of flowering plants during the Albian Age of the Gallic Epoch of the early Cretaceous Period are inconsistent with molecular-based phylogenies of Coleoptera that suggest a Triassic origin of certain non-chrysomelid beetle lineages.
When taking into account the cyclic nature of angiospermization, flowering plants as traditionally defined, are a loose amalgam of parallel evolutionary lines traceable to surviving geographically disparate Early Triassic remnants of already divergent Permian seed plant lineages.
[ Discussion of the Thigmomorphogenetic/Coevolutionary Hypothesis ]
I now consider and discuss evidence drawn from plant anatomy and development, ecology, physiology, and genetics, which is critical in understanding the origin of flowering plants. Throughout this essay I adopt the integrative biologic approach, which is subject to periodic revision. Adjustments and refinement | | |
