"gigantopterid" = an English noun describing large leaves with complex reticulate venation resembling the Cathaysian fossil seed plant genus Gigantopteris and North American genus Delnortea of the Permian Period, 260 million years ago"

You are here: Paleobotany of Angiosperm Origins

ESSAY CONTENTS


[ Paleobotany of Angiosperm Origins ]

JOHN M. MILLER, Ph.D.

University and Jepson Herbaria
Room 1001, Valley Life Sciences Building 2465
University of California, Berkeley
Berkeley, California, USA 94720-2465



Having discussed the origin of angiosperms from shrub-like Carboniferous or Permo-Triassic seed plant stock I outline and discuss the evolution of seed plants and biodiversity and paleontology of extinct Paleozoic lignophytes and their phytophagous insect associates, which is necessary to solve the riddle of angiosperm beginnings within a coevolutionary and phylogenetic context.

"... 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 quoted 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.

Is there convincing fossil evidence of the first flowering plants or their antecedents? No, according to E. L. Taylor and T. N. Taylor (2009).

This second of three essays states potential challenges from paleobotanical research perspectives, surveys the main groups of seed plants most often discussed as possible ancestors of flowering plants, diagrams a hypothetical protoflower of a Paleozoic gigantopteroid seed plant, which is concordant with the latest models of gene expression and fertile shoot apical meristem (SAM) evolutionary development (evo-devo), and concludes with brief homology assessments, character matrixes, and student problems needed to practice phylogenetic analyses and to learn new skills.

High points and major milestones in paleoentomology are discussed in the following essay to include a brief outline of arthropod assemblages, paleoecology, taphonomic factors, stem groups, and the systematics and paleobiology of Conrad Labandeira's "Big Five" pollinators and palynivores.

Key points in a discussion of arthropod evo-devo and insect physiology are presented in the first essay on the origin of angiosperms.

Based upon knowledge gained from SAM models of homeodomain proteins and deeply conserved LEAFY (LFY) transcription factors (TFs) did hermaphroditic protoflowers evolve long before cupules and associated axillary organs of Caytoniales? Yes.

Bisexual strobili are the focus of the leading model of cone and floral organization (Melzer et al. 2010). Several recent studies of developmental abnormalities in cones of extant conifers offer students another angle for better understanding the origins of flowers and flower-like organs and character homologies (Flores-Rentería et al. 2011, Rudall et al. 2011).

Further, there is little or no support in the fast-moving literature on tool kits for past proposals on the evo-devo of angiosperm ovules and carpels from cupules and axillary organs of Mesozoic Caytoniales. Simply put, pteridosperm cupules probably had nothing to do with the origin of angiosperms.

"The extended presence of bisporangiate cones throughout the gymnosperms reflects the possible existence of a genetic mechanism similar to that of angiosperms."

The above quotation is from page 136 of L. Flores-Rentería, A. Vásquez-Lobo, A. V. Whipple, D. Piñero, J. Márquez-Guzmán, and C. A. Domínguez (2011), Functional bisporangiate cones in Pinus johannis (Pinaceae): implications for the evolution of bisexuality in seed plants. American Journal of Botany 98(1): 130-139.

The image on the upper right-hand side of the page is the distal end of the largest known specimen of the Paleozoic gigantopteroid seed plant, Delnortea abbottiae, United States National Museum (USNM) specimen number 387473, photographed by the author in 1982 on the same day the fossil was unearthed from beds of the Lower Permian Cathedral Mountain Formation of the Del Norte Mountains of southwestern North America. It is published as Figure 18 on page 1413 of Mamay et al. (1988).

I suggested in the first essay on the origin of angiosperms that one "reciprocal mechanism" sensu Crepet and Niklas (2009) leading to diversification of the stem lineage(s) of flowering plants and holometabolous insects was potentially linked with global hypoxia (low pO2) and temperature extremes induced by three or more mass extinctions during the past 300 million years.

The most severe global apocalypse of all time, which might have been a critical bottleneck in the evolution of flowering plants and Holometabola, was the end-Permian extinction (EPE).

Extreme temperatures and global hypoxia potentially unleashed moult cycles resulting in novel anterior and thoracic larval development in clades of early holometabolous insects that inhabited shrub lifeboats and whole lignophyte organs including cone-bearing seed plant SAMs.

Further, I hypothesized that phytoecdysones secreted by Permo-Carboniferous and Permo-Triassic shrub lifeboats potentially affected body size and moulting time of phytophagous insect antagonists. The reverse was also suggested, namely that baculoviruses of insect vectors passed along transposable elements (TEs) to shrub lifeboats potentially affecting biosynthesis of cone and floral tool kit proteins.

The previous essay placed an interesting idea on the table, namely, that molecular coevolution of insect and seed plant cis-regulatory modules (CRMs) and early diverging developmental tool kits probably took place in shrub lifeboat-phytophagous insect compartments indigenous to biomes of the Carboniferous icehouse and later Permian hothouse Earth.

Ancient WGDs are implicated in both the common ancestor of eudicots and monocots and in the MRCA roughly coinciding with the Frasnian-Famennian ice-house (DeCARB) and Triassic-Jurassic carbon cycle event (TrCCE). Further, an exhaustive genomic study of the cultivated grape overwhelmingly supports the existence of paleohexaploidy (Jaillon et al. 2007), which is equivalent to the "γ triplication" cited by Jiao et al. (2011).

Based on a trail of biochemical clues gleaned from studies of vegetative growth and SAM organization in extant model lignophytes and monilophytes, when combined with insight gained from molecular phylogenetic analyses of class III homeodomain leucine zipper (Class III HD-Zip) genes and KNOTTED1 homeobox TFs at least two or more evo-devo programs might have existed in early diverging Devonian progymnosperm and seed plant populations.

I also proposed in the first essay on the origin of angiosperms that modern models of SAM trafficking of mobile cis-acting homeodomain TFs and certain promoters, enhancers, messenger RNAs, and phytohormones may be used to simplify morphological phylogenetic analysis of seed plants, or to conduct certain cladistically based experiments.

This approach was adopted in the present exercise. Finally, I suggested that cladogenesis of flowering plants may be traced back in geologic time to the EPE, and to surviving remnants of already divergent Permian seed plant lineages.


Paleobotanical Challenges and Choices:

By knowing the interval in geologic deep time when molecular systematists predict divergence of reproductive patterning genes and regulatory proteins, paleobotanists might be able to better focus on candidate seed plant groups for detailed anatomical study of permineralized fossils (Crepet 2008). A book chapter written by David Winship Taylor (2010) seemingly adopts these approaches.

Further, ancient WGDs are implicated in both the common ancestor of eudicots and monocots and in the MRCA (Jiao et al. 2011). Paleobotanists should contribute data to efforts refining the timing of WGDs by suggesting suitable guide fossils to be used in calibrating the timing of α, β, and γ WGDs.

An exposure of the Triassic (Norian) Chinle Formation in the Petrified Forest National Park of southwestern North America is pictured to the right, which contains massive weathered log fragments of Araucarioxylon arizonicum.

Identifying the whole plant morphology and evolutionary relationships of the gymnosperm that produced this fossil is a paleobotanical challenge.

The image was captured by T. Scott Williams, Park Curator and Photographer, and is reproduced here with his permission.

But do paleobotanists pay attention to proposals of plant biologists and molecular phylogeneticists, and vice versa? Yes.

Should paleobotanists coordinate a concerted effort with developmental biologists to reevaluate fossils, "... to identify fingerprints of developmental regulation for a broad spectrum of plant structures," as stated by Sanders et al. (page 723, 2007)?

Telombs, trusses, and potentially tantalizing questions. Zimmermann's Telomb Theory has figured prominently in discussions by paleontologists and plant morphologists on the origin of megaphylls or true leaves (Stewart and Rothwell 1993, Stein and Boyer 2006, Beerling and Fleming 2007, Sanders et al. 2007). The origin and evolution of the megaphyll is reviewed in a paper by Galtier (2010).

Yet, "... no single plant lineage has been found to exhibit all three crucial steps [overtopping, planation, webbing] in its fossil history" (page 5, Beerling and Fleming 2007). Remarks in brackets [] are mine.

The planar megaphyll illustrated at the beginning of this essay, which was described by Mamay et al. more than twenty years ago (1988) shows exquisite details of webbing in a gigantopterid leaf with four orders of venation. Can paleobotanical and phylogenetic studies of transformational series in Delnortea and other late Paleozoic gigantopteroid seed plants shed light on classic tenets of plant morphology such as Zimmermann's Telomb Theory or Arber and Parkin's Strobilus Theory of the Angiospermous Fructification?

  • What were the whole plant morphologies and architectural innovations of Devonian, Carboniferous, and Permo-Triassic seed plants?
  • Can we identify adaptations (anatomic, biochemical, physiologic, and morphologic) of Paleozoic gigantopteroids and other enigmatic groups possibly exploited by Permo-Triassic animals and other organisms?
  • Are Phasmatocycas bridwellii ovule-bearing megasporophylls and (undescribed) microsporangia-bearing microsporophylls, the detached remains of gigantopteroid plants with a gigantic bracteopetaloid perianth attached the bisexual cone axis of an enormous proanthostrobilus?
  • If bisexual strobili are the focus of most of the leading models of cone and floral organization (Melzer et al. 2010), how can we reconcile studies of developmental abnormalities in cones of extant conifers (Flores-Rentería et al. 2011, Rudall et al. 2011) with classical hypotheses published by Arber and Parkin (1907), Hamshaw Thomas (1925), and J. A. Doyle (1978)?
  • "Which type of carpel found in living taxa is most similar to the ancestral form" ... (page 120, D. W. Taylor and Kirchner 1996)?
  • "What is the ancestral number of ovules" ... (page 120, D. W. Taylor and Kirchner 1996)?
  • "Why is there variability among carpels in the basal angiosperms" ... (page 120, D. W. Taylor and Kirchner 1996)?
  • "What are the transformations among carpel types" ... (page 120, D. W. Taylor and Kirchner 1996)?
  • "What controls produce the carpel wall and the placenta" (page 155, D. W. Taylor 2010)?
  • Based upon data to be gathered on the stratigraphic distribution of oleananes and plant fossils, did Paleozoic seed plants manufacture and use steroids, resins, and terpenoids as defense against herbivores?
  • If supported by studies of trace molecules in permineralizations of Paleozoic seed plants, could phytoecdysones potentially signal the hemocyanin, juvenile hormone (JH), and vitellogenin developmental tool kit of invertebrate antagonists residing in shrub lifeboats?
  • Do vojnovskyalean fossils yield oleananes?
  • As ascertained by analysis of geochemical/isotopic data from studies of carbonates and fossil soils, and biostratigraphic evidence, was it likely that oxygen-generating Permo-Triassic seed plants existed in hypoxic, carbon dioxide-, and methane-rich terrestrial paleoenvironments, coevolving with respiring colonies of intimate invertebrate mutualists and populations of physiologically-stressed tetrapods?
  • Could coevolving insect colonies inhabiting Permo-Carboniferous and Permo-Triassic shrub lifeboats environmentally or epigenetically affect SAM tool kits and accessory fertile meristems leading to developmental recombination via reproductive modules, genetic accommodation, and the eventual spread of adaptive phenotypes in pre-angiospermous populations?
  • What were the insect groups of Herbivore Expansion Phase 2 that exploited Carboniferous and Permian seed plants?
  • Can we examine the gut contents of fossilized Mesozoic beetles and sphecid wasps to find evidence of their interactions with flowering plants as suggested by Grimaldi (1999)?
  • Can we compute dendrograms of phytophagous insects, which are calibrated and complimentary to revised phylogenetic reconstructions of specific seed plant host lineages to include Vojnovskyales?
  • Does a phylogenetic signal left behind by the original inhabitants of Permo-Triassic shrub lifeboats exist as ascertained through study of phytophagous insect antagonists of extant seed plants?
  • Pending discovery and paleobotanical study of additional permineralized reproductive material of Paleozoic gigantopteroids and vojnovskyaleans can we revise phylogenetic reconstructions of extinct seed plant lineages to pinpoint and refine the late Paleozoic divergence(s) of angiosperms from the MRCA?
  • With the possibility in mind that certain Permo-Triassic gymnosperms might be angiophytes (Stockey and Rothwell 2009), which group(s) gave rise to the angiosperm clade(s)?
  • "Do the angiosperms show as rapid an evolution as Darwin believed when he wrote about the abominable mystery" ... (page 324, Stockey and Rothwell 2009)?
  • "How do we distinguish true angiosperms from angiophytes in the fossil record" ... (page 324, Stockey and Rothwell 2009)?
  • "Are the lines [of evolution among angiophytes] beginning to blur"... (page 324, Stockey and Rothwell 2009)? (phrase in [] brackets is mine)
  • Assuming calibrated relaxed clock methods (e.g. Magallón 2010, Stephen A. Smith et al. 2010) are more precise than other approaches, and posit a Paleozoic origin of angiosperms, conifers, cycads, ginkgos, and gnetophytes, how is it possible that certain Mesozoic pteridosperms are basal to stem group flowering plants?
  • Taxon-specific biomarkers (TSBs). A first clue to the mysterious origin of angiosperms comes from geochemical studies of taxon-specific biomarkers (TSBs) isolated and characterized from coal balls (Moldowan and Jacobson 2002). Taxon-specific biomarkers include naturally occurring but fossilized triterpenoids known as oleanone triterpanes (oleananes). Oleananes, together with ursenes, lupenes, and taraxerenes are important TSBs that belong to a class of β-amirin triterpenoids (Moldowan and Jacobson 2002).

    Oleanane TSBs have been recovered and characterized from Permian gigantopterid seed fern compressions (D. W. Taylor et al. 2006). A weak oleanane signal was found in Carboniferous rocks but the plant that produced the molecular tracer is unknown (D. W. Taylor et al. 2006).

    Gigantopterids are known from Carboniferous and Permian leaf compression floras. Permineralizations of reproductive material are rare and require detailed study. Whole plant morphology of gigantopterids is unknown. Surprisingly, oleananes are also found in sedimentary rock compressions of Jurassic bennettitaleans and Cretaceous "dicotyledonous" flowering plants (D. W. Taylor et al. 2006).

    Despite these considerable gaps in our knowledge of Paleozoic gigantopterids and solid geochemical evidence that points toward a possible evolutionary connection with bennettitaleans and "dicotyledonous" flowering plants, Glasspool et al. (2004) state:

    "Additional similarities [to eudicot flowering plants] in the presence of water conductive vessels capable of sustaining similar physiological conditions, lead us to consider gigantopterids to be vegetative analogues of angiosperms."

    The above quotation is from page 105 of I. J. Glasspool, J. Hilton, M. E. Collinson, S.-J. Wang, and L.-C. Sen (2004), Foliar physiognomy in Cathaysian gigantopterids and the potential to track Palaeozoic climates using an extinct plant group, Palaeogeography, Palaeoclimatology, Palaeoecology 205: 69-110. Remarks in brackets [] are mine.

    What is the simplest scientific explanation why some Permian gigantopterids would yield the same oleanone triterpanes as Cretaceous "dicotyledonous" angiosperms and bennettitaleans?

    Floral paedomorphism and coevolving body allometries. Controversial assertions having to do with the origin of angiosperms abound in the scientific literature of the 20th century and three categories of credible hypotheses and theories exist (Rothwell et al. 2009). With the exception of Takhtajan's neglected hypothesis on a "neotenous origin of flowering plants" (page 209, 1976), none of these ideas when taken as a whole are neither compelling or plausible to many scientists, including the author.

    Can paleobotanists formulate explicit hypotheses on the origin of flowering plants based on principles of paedomorphic heterochrony? The best starting point for students of neoteny and paedomorphism is the classic work of S. J. Gould (1977).

    Advanced paleobotany students should study phylogenetic methods and tests proposed by Larry Hufford (2002), which are needed to detect heterochrony.

    A reconstructed bennettitalean flower, which is classified as Williamsonia harrisiana appears to the left. 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,' based on Bose (1968, pl. 1, figs. 8, 9); × 1.5."

    Can paleoentomology provide data of potential use in predicting the allometric scaling relationships between certain stem group Paleozoic insects such as palaeodictyopterans and panorpoids; and the proanthostrobili, microsporangia, and ovules they potentially visualized and ate?

    From the research perspective of paleoentomology and floral origins, allometric scaling data might be applied to understanding potentially interesting macroevolutionary aspects of paleoecology and insect/seed plant organ development tied-in with molecular coevolution of HTH homeodomain proteins.

    Interestingly, the arthropod homeodomain protein Engraled shares a similar HTH tertiary enzyme structure to LFY protein, which is necessary for cone and floral development (Hamès et al. 2008).

    Did hypothetical proanthostrobili of certain Paleozoic seed plants simply get smaller and more condensed ("evolutionary juvenilization," [page 699, E. O. Guerrant, Jr. 1982]) over the course of many millions of years together with their coevolving insect antagonists through the process of paedomorphic heterochrony?

    If proven correct by paleobotanical studies, enormous Paleozoic protoflowers 20 cm or more in diameter, might constitute the plesiomorphic condition for angiosperms, in contrast to tiny flowers recovered from Cretaceous sediments (Friis et al. 2005, Friis et al. 2006), regarded by certain workers as ancestral, basal, early, and early-divergent forms.

    Angiosperms were certainly not the only seed plants that possessed flowers or flower-like reproductive structures, as the preceding figure caption suggests. Flowers are found in bennettitaleans and certain gnetophytes such as Welwitschia (Friis et al. 2006). Certain extant Hydatellaceae produce non-flowers (Rudall et al. 2009).

    "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."

    The preceding statement is from the abstract on page 3471 of R. A. Bateman, J. Hilton, and P. J. Rudall (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.

    I argue that no "assembly" (page 816, J. A. Doyle 2008) of perianth parts, microsporophylls, and megasporophylls to form a flower was necessary. Simply put, massive bisexual cone axes with a spirally arranged perianth and whorls of microsporophylls and megasporophylls growing from fertile spur shoot SAMs probably already existed in populations of poorly understood Paleozoic seed plants described as gigantopteroids and Vojnovskyales, groups omitted by J. A. Doyle and others in their many published phylogenetic analyses.

    Implications of a paper by Axsmith et al. (2003) that reconsiders the Paleozoic gymnosperm Phasmatocycas bridwellii were ignored in all published contributions on the origin of flowering plants appearing in the 2009 Charles Darwin Bicentennial Issue of the American Journal of Botany. Brian Axsmith and coworkers reinterpret the anatomy, morphology, and taxonomic placement of phyllospermous Carboniferous leaf fragments first described as spermopterids (see discussion in later sections of this essay).

    I ask the straightforward question:

    Were some of the detached spermopteroid megasporophylls found in the same bedding planes where delnorteas and evolsonias are found (Mamay et al. 1984, Mamay 1989, Ricardi et al. 1999, DiMichele et al. 2000) actually detached pieces of much larger 300 million year old bisexual protoflowers of a completely new kind of gigantopteroid seed plant?

    Based on molecular phylogenetic-, homeotic gene expression-, and tool kit studies, S. Kim et al. (2004), Baum and Hileman (2006), and Theißen and Melzer (2007), predict the existence of hypothetical protoflowers, complete with leaf-like heteroblastic microsporophylls and sterile bracteopetaloid perianth parts attached to elongated bisexual cone axes.

    Gigantopteroid seed plants and Vojnovskyales are discussed as two potential ancestors of the angiosperms in the next several chapters, while drawing attention to possible coevolution of phytophagous insects with developmentally plastic Carboniferous and Permian vascular plant stock. Arthropod and seed plant assemblages (Labandeira 2000) are also reviewed and tied-in with a brief survey of accomplishments in paleoentomology and the high points of studies in insect molecular systematics.

    What are the seed plant and arthropod groups upon which to base a study of the origin and evolution of stem group angiosperms and holometabolous insects, and the derived crown orders?

    As global atmospheric oxygen levels plummeted during the DeCARB, invertebrate hexamerin food storage and moulting proteins diverged in Plecopteran (stonefly) ancestors leading to several clades of hemimetabolous and holometabolous insects (Hagner-Holler et al. 2007).

    How is the molecular evolution of hexamerins tied-in with deep time heterochronies in hemimetabolous Isoptera and Mecoptera, and the evolution of caste polyphenism in holometabolous ants, bees, and wasps?

    Coevolving arthropod antagonists of Permo-Carboniferous and Permo-Triassic seed plants potentially inhabited vegetation compartments including fragmented biomes and miniature habitats within massive SAMs, cone axes, and crevices of leaf bases, bark, and wood. A considerable body of paleontologic data has already been assembled on relationships between Paleozoic arthropods and vascular plants (Krassilov 1997, Labandeira 1998, Rasnitsyn 2002).

    Innovative seed plants of unstable extrabasinal paleoenvironments might have included gigantopterids (Mamay et al. 1988) and Vojnovskyales (Rothwell et al. 1996).

    The Carboniferous Period, well known for its coal swamp flora and fossil insects, is also the time when extrabasinal habitats "may have served as cradles for major evolutionary innovations ..." (page 1077, Rothwell et al. 1996).

    Concepts developed in my first essay are reminiscent of proposals on a Cretaceous or Jurassic origin of angiosperms (Hughes 1976), but postulate a coevolution of flowering plant antecedents with phytophagous arthropod antagonists to the much older Carboniferous and Permian Periods of the Paleozoic Era.

    When in geologic time do we mine the rocks looking for paleobotanical evidence of the ancestors of flowering plants?


    Paleontologic Evidence:

    I now summarize evidence from a paleontologic research perspective to support of a coevolutionary origin of angiosperms and certain arthropod groups. The chapter is split into two sections: the paleobotany of gymnospermous seed plants and a second on the paleoentomology of insect groups which might have ate, bred, and sheltered inside Paleozoic and early Mesozoic vegetation compartments.

    Paleobotany of seed plants. The brief history of major seed plant groups outlined in the next section is distilled from review papers and books by Crane (1985), Stewart and Rothwell (1993), Rothwell and Serbet (1994), Krassilov (1997), E. L. Taylor et al. (2006), Mendes et al. (2008), E. L. Taylor and T. N. Taylor (2009), and T. N. Taylor et al. (2009).

    You may navigate away from this page to other sections of the discussion by following the underlined hot links in the bulleted list below. Three of the seed plants groups listed below, gigantopterids, Phasmatocycas, and Sanmiguelia are not placed in a specific taxonomic order because an appropriate name is unavailable or not validly published.

    The major taxonomic orders of seed plants according to T. N. Taylor et al. (2009) and others, except flowering plants are:

  • Bennettitales
  • Callistophytales
  • Caytoniales
  • Coniferales
  • Cordaitales
  • Corystospermales
  • Cycadales (including Nilssoniales)
  • Czekanowskiales
  • Erdtmanithecales
  • Gigantopterids
  • Ginkgoales
  • Glossopteridales
  • Gnetales
  • Hermanophytales
  • Hydrospermales
  • Iraniales
  • Lagenostomales
  • Phasmatocycas (spermopterids Incertae Cedis)
  • Peltaspermales
  • Pentoxylales
  • Petriellales
  • Sanmiguelia (Order Incertae Cedis)
  • Taxales
  • Trigonocarpales
  • Vladimariales
  • Vojnovskyales
  • Voltziales
  • Callistophytales (Rothwell 1981), Czekanowskiales (X.-Q. Liu et al. 2006, C. Sun et al. 2009), Erdtmanithecales (Mendes et al. 2008, Friis et al. 2009, Mendes et al. 2010), Ginkgoales (Jager et al. 2003, Zhou and Zheng 2003, Zheng and Zhou 2004, Zhou 2009, Bugdaeva 2010, Feng et al. 2010, Fischer et al. 2010, Golovneva 2010, Nosova and Kiritchkova 2010), Hermanophytales (see T. N. Taylor et al. 2009), Iraniales (see T. N. Taylor et al. 2009), Peltaspermales (Booi et al. 2009, E. L. Taylor and T. N. Taylor 2009, Bomfleur et al. 2011), Petriellales (E. L. Taylor et al. 2006, E. L. Taylor and T. N. Taylor 2009), and Vladimariales (Gordenko 2010) are also important groups needed to better understand seed plant evolution.

    Bennettitales, Caytoniales, Czekanowskiales, Gigantopteridales, Glossopteridales, and Pentoxylales are the main seed plant groups of focus in elucidating the origin of angiosperms according to the most comprehensive treatise on paleobotany (T. N. Taylor et al. 2009).

    Two additional groups of Paleozoic gymnosperms are included in my discussion on the origin of the flowering plant stem group: Phasmatocycas bridwellii because these fossils might be megasporophylls of enormous gigantopterid protoflowers and, (2) Vojnovskyales since they possess bisexual cone axes that fit evo-devo models of flower origins published by Baum and Hileman (2006), Theißen and Melzer (2007), and Melzer et al. (2010).

    Table 2 outlines the Paleozoic and Mesozoic fossil history of the main taxonomic orders of seed plants based on Stewart and Rothwell (1993), Friis et al. (2009), and T. N. Taylor et al. (2009).

    A proposal to classify land plants by Chase and Reveal (2009) is not adopted in this essay because of incompleteness (but is followed in the third essay on Evolution of Mesozoic Angiosperms).

    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 Period of the Cenozoic Era.


    Table 2. Fossil History of the Provisional Orders of Seed Plants (Excluding Flowering Plants).

    Order

    Devonian

    Carboniferous

    Permian

    Triassic

    Jurassic

    Cretaceous

    Bennettitales

    0

    0

    0

    6(8)

    6(8)

    6(9)

    Callistophytales

    0

    3(12)

    2(2?)

    0

    0

    0

    Caytoniales

    0

    0

    0

    1?

    3(4)

    3(4)

    Coniferales

    0

    0

    0

    9(11)

    9(11)

    46

    Cordaitales

    0

    2(9)

    2(9)

    0

    0

    0

    Corystospermales

    0

    0

    1?

    3(16)

    3(16)

    3(16)

    Cycadales (including Nilssoniales)

    0

    0

    2

    3

    1(3)

    1(3)

    Czekanowskiales

    0

    0

    0

    1

    5

    5

    Erdtmanithecales

    0

    0

    0

    0

    0

    5

    Gigantopteridales and Gigantonomiales

    0

    1?

    8(10)

    ?

    0

    0

    Ginkgoales

    0

    0

    1?

    8(3)

    8(3)

    8(3)

    Glossopteridales

    0

    0

    1(9)

    ?

    ?

    0

    Gnetales

    0

    0

    1

    6

    6

    7

    Hermanophytales

    0

    0

    0

    0

    1

    1

    Hydrospermales

    4(6)

    0

    0

    0

    0

    0

    Iraniales

    0

    0

    0

    1

    0

    0

    Lagenostomales

    1(14)

    1(14)

    1(14)

    0

    0

    0

    Peltaspermales

    0

    >1

    3(16)

    3(16)

    ?

    ?

    Pentoxylales

    0

    0

    0

    0

    1

    ?

    Petriellales

    0

    0

    0

    1

    0

    0

    Phasmatocycas (spermopterids)

    0

    2

    5

    ?

    0

    0

    Sanmiguelia (Incertae Cedis)

    0

    0

    0

    1

    0

    0

    Taxales

    0

    0

    0

    0

    1

    1(3)

    Trigonocarpales

    4(22)

    4(22)

    4(22)

    0

    0

    0

    Vladimariales

    0

    0

    0

    0

    1

    0

    Vojnovskyales

    0

    1(1)

    3

    0

    0

    0

    Voltziales

    0

    1(8)

    1(8)

    1(8)

    1(8)

    0


    Arthropod assemblages: paleoentomology of palynivores and pollinators. Earlier, I proposed that Permo-Carboniferous and Permo-Triassic arthropods including forerunners of holometabolous insects formed close but antagonistic associations with seed plant shrub lifeboats. Paleozoic vegetation compartments and shrub lifeboats might be viewed as potential venues where seed plant and insect coevolution took place under selective forces of hypoxia and temperature extremes.

    Was hypoxia (low pO2) a powerful selective force on paleopopulations of interacting arthropods and land plants? Yes.

    Based on studies published by protein biochemists (Burmester 2004), I concluded that molecular evolution of invertebrate hemocyanin (Hc) enzymes and their derived insect hexamerins (Hxs) was probably driven by the rise and fall of oxygen in the Earth's atmosphere at two intervals during the Paleozoic Era. Phytophagous insects might have used oxygen generating vegetation compartments of hypoxic fitness landscapes as a source of food and for shelter from cold and ultraviolet (UV) radiation.

    Insect-seed plant interactions affected by temperature extremes and global hypoxia in Paleozoic terrestrial biomes probably led to diversification at the molecular level in early seed plant and holometabolous insect lineages and evo-devo of flowers from bisexual cone axes following the Baum and Hileman hypothesis (2006) and refined models of cone and floral SAM evo-devo by Theißen and Melzer (2007) and Melzer et al. (2010).

    Intriguing interactions among microbes and viruses, mycorrhizal fungi, phytophagous insects, and seed plants residing within coevolutionary compartments, which I termed shrub lifeboats in the first essay, might have involved ecdysteroid signalling, thigmo, and cross-Kingdom movement of chromosome parasites, specifically TEs of the LTR retrotransposon type.

    The adult butterfly pictured above has reached the final days of its brief life.

    Paleontological data are gleaned from studies of coal balls (Labandeira et al. 1997), preserved plant organs (pollen, spores, seeds) and detached plant parts (often with insect traces). Insect frass, permineralized gut contents, and fossilized mouthparts and ovipositors are often critically important sources of paleobotanical and paleoentomological data.

    Key reviews by Labandeira (1997, 1998, 2000, 2010) outline the main kinds of paleontological evidence that have been useful in gaining insight on the close associations between arthropods and vascular plants in deep time.

    The treatise on the anatomy, morphology, phylogenetic relationships, physiology, and fossil history of insects is Grimaldi and Engel (2005).

    A book on fossil insects edited by Rasnitsyn and Quicke (2002) is a cornerstone reference on paleoentomology.

    While reviewing the paleobiology of pollination, Conrad Labandeira (2000) developed the concept of insect-plant "evolutionary assemblages." These assemblages are:

  • Assemblage 1: Primitive Vascular Plants and Unknown Arthropods
  • Assemblage 2: Ferns, Seed Plants and the Paleozoic Insect Fauna
  • Assemblage 3: Seed Plants and the Earlier Phase of Modern Insect Fauna
  • Assemblage 4: Angiosperms and the Later Phase of the Modern Insect Fauna
  • Key review papers, books, and book chapters on insect classification and phylogeny, paleoentomology, and paleobiology of arthropod associations with plants are Wootton (1981), Lawrence and Newton (1982), Wootton (1990), Labandeira et al. (1994), Labandeira and Phillips (1996), Labandeira et al. (1997), Labandeira (1997, 1998, 2000), Wilf et al. (2000), Dmitriev and Ponomarenko (2002), Labandeira (2002), Labandeira et al. (2002), Whiting (2002), Zherikhin (2002), Béthoux et al. (2005), Grimaldi and Engel (2005), Labandeira (2006, 2007), Labandeira and Allen (2007), and Labandeira (2010).

    Students of insect systematics will enjoy accessing Royal Entomological Society "virtual issues" of Systematic Entomology. These include a 2009 electronic volume on fossil insects and the 2010 online edition on bee systematics.

    Taphonomic factors in paleoentomology. A discussion of the paleoentomology of arthropods is not possible without brief mention of the taphonomic factors that lead to burial and preservation of insect remains. Taphonomic factors listed by Zherikhin (2002), which are critical in understanding the paleoentomology of insect origins include:

  • Autotaphonomical factors (presence of a hydrophobic chitenous exoskeleton, moulting by ecdysis, shedding of wings and elytrae from adult carcasses)
  • Ecological factors including relative abundance of arthropods in paleoenvironments over other forms of life
  • Mortality and taphotopical factors which have a bearing on biostratigraphy and frequency of burial of Lagerstätten
  • Depositional environments (post-mortem ecological factors)
  • Post-burial factors including diagenesis of fossilized remains
  • Technical factors (too few paleoentomologists to mine and describe the fossils)
  • Biostratigraphic considerations and selectivity of the rock record
  • Ecological factors in paleoentomology. The main functional feeding groups of insects deduced from paleontologic evidence are:

  • External foliage feeders
  • Piercers and suckers
  • Borers
  • Galling insects
  • Leaf miners
  • Sporiovores
  • Pollenivores
  • Surface fluid feeders
  • Fossil history of arthropod antagonists of lignophytes. As the Earth slowly warmed following the DeCARB, "Assemblage 2: Ferns, Seed Plants and the Paleozoic Insect Fauna" became discernable in the fossil record (Labandeira 1998, 2000, 2006).

    Rocks of the Carboniferous and Permian Periods from widely separated localities yield fossils of Ephemeroptera (mayflies), Palaeodictyoptera (extinct), Plecoptera (stoneflies), Dermaptera (earwigs), Grylloblattodea (ice-crawlers), Caloneurida (extinct), Orthoptera (crickets, grasshoppers, katydids), Dictyoptera (cockroaches, mantises, termites), Lophioneurida (including psocids and bark lice), Hemiptera (plant lice, true bugs), and Coleoptera (beetles and weevils) (Table 3, below; Table 4.24, page 146, Grimaldi and Engel 2005).

    Pollen- and pollenkitt-eating insects of Paleozoic Assemblage 2 included several extinct families of Grylloblattodea; hypoperlids, and psocids. Gut contents of these insects consisted of palynomorphs assignable to extinct voltzialean conifers, cordaitaleans, glossopterids, gnetaleans, and peltaspermaleans (Labandeira 2000).

    Paleozoic phytophagy was not only confined to ovules, pollen, pollenkitt, seeds, spores, and wood. Gigantopterid leaves were also eaten by insects (Beck and Labandeira 1998, Glasspool et al. 2003). Foliage representing the remains of several vascular plant groups was evidently part of the diet of Permo-Carboniferous insects (Labandeira 1998, 2006).

    The resurgence of terrestrial animal and plant life recovering from the EPE probably led to evolution of the first seed plant pollinators (Cornet 1989). Labandeira (2000) identifies these (and other) insect-plant mutualisms as "Assemblage 3: Seed Plants and the Earlier Phase of Modern Insect Fauna," which are based on his review of paleontologic evidence from insect mouthparts and gut contents, and seed plant reproductive organs.

    Data summarized in Table 3 (below) show the extinction of the Palaeodictyoptera and Caloneurida coupled with the appearance of the five new insect orders: Emboidea (appearing in the early Cretaceous Period), Thysanoptera, Hymenoptera (ants, bees, and wasps), Diptera (flies, Figure 306, page 230-231, Rasnitsyn 2002), and Lepidoptera.

    The early fossil history of the main taxonomic orders of arthropod antagonists of seed plants presented in this essay is distilled from data published in Rasnitsyn (2002), Grimaldi and Engel (2005), and Labandeira (2006). Groupings of higher categories of arthropods follow the taxonomic scheme illustrated by Grimaldi and Engel (Figure 4.24, page 146, 2005). Some of the insect orders are lumped together as super orders, depicted in bold type in the table below.

    Integers in each cell of Table 3 represent the number of insect families reported from the fossil record boiled down from discussion in Rasnitsyn (2002) including data on non-insect hexapods from Grimaldi and Engel (2005). A question mark [?] in a cell denotes gaps in the data due to controversial or uncertain familial taxonomic placement. Ghost lineages are illustrated in the table by a white space with a question [?] mark spanning a particular geologic period.


    Table 3. Paleozoic and Mesozoic Fossil History of the Main Arthropod Orders of Vascular Plant Antagonists.

    Order

    Devonian

    Carboniferous

    Permian

    Triassic

    Jurassic

    Cretaceous

    Archaeognatha

    ?

    1

    1

    ?

    ?

    2

    Caloneurodea

    0

    3?

    5

    0

    0

    0

    Coleoptera

    0

    1

    6?

    20?

    35

    >35

    Collembola

    1

    ?

    ?

    ?

    ?

    1

    Dermaptera

    0

    0

    2

    1?

    2

    3?

    Dictyoptera

    0

    7

    7

    6?

    3?

    9

    Diptera

    0

    0

    0

    16?

    29?

    36?

    Emboidea

    0

    0

    0

    0

    0

    1?

    Ephemeroptera

    0

    3

    2

    1

    2

    4

    Grylloblattodea

    0

    2

    32

    11

    4

    2

    Hemiptera

    0

    0

    10

    16?

    28

    >37

    Hymenoptera

    0

    0

    0

    1

    18

    57?

    Lepidoptera

    0

    0

    0

    0

    4

    10

    Lophioneurida

    0

    0

    2?

    2?

    2?

    1

    Orthoptera

    0

    1

    3

    8

    9

    9

    Palaeodictyopterida

    0

    14

    5

    0

    0

    0

    Plecoptera

    0

    0

    6

    4

    6

    8

    Thripida

    0

    0

    0

    1?

    4

    >6

    Zygentoma

    0

    ?

    ?

    ?

    ?

    2


    Based on scanty paleontologic evidence the basal arthropod orders Collembola (springtails), Archaeognatha (bristletails), and Zygentoma (firebrats or silverfish) probably co-occurred with the earliest divisions of vascular plants (Rhyniophyta, Trimerophytophyta, and Zosterophyllophyta; Table 1, page 350, Labandeira 1998; Table 1, page 415, Labandeira 2006). Myriapods (centipedes and millipedes) probably also fed on detritus associated with Silurian and early Devonian algae, fungi, and the first vascular plants (Labandeira 1998).

    Spores were probably consumed by the earliest arthropods and other detritivores. The Silurian and early Devonian Periods are the points in geologic time when "Assemblage 1: Primitive Vascular Plants and Unknown Arthropods" once existed (Labandeira 2000).

    Ponomarenko (2009) reviews the contributions of Paleozoic arthropods toward development of terrestrial biomes. Coal ball permineralizations provide an extensive record of oribatid mite detrivory, mite body fossil occurrences, and evidence of insect borers, which were indigenous to Carboniferous forested swamps of North America (Labandeira et al. 1997).

    There was an explosion of evolutionary diversity of Hymenoptera following the EPE, beginning with the appearance of the basal family Xyelidae in the Triassic Period (Figure 331, page 244-245, Rasnitsyn 2002). Sawflies are often preserved in the rock record together with their pollen loads (Krassilov et al. 2003).

    Labandeira's "Assemblage 4: Angiosperms and the Later Phase of the Modern Insect Fauna" is discussed in the third essay on Mesozoic Paleobiodiversity of Angiosperms, which is located elsewhere on this web site.

    Adaptive radiation of at least some of the pollen- and nectar-feeding insect orders following the EPE is probably attributable to evo-devo of innovative mouthpart anatomy (Labandeira 2010). Specific feeding adaptations were first seen in fossil flies (labellar modifications for sponging of pollen and seed plant rewards), moths (siphons for nectar and secretions), and wasps (clasping structures used to collect pollen) (Labandeira 2000).

    Arthropod stem groups. Evolutionary developmental, genetic, molecular phylogenetic, and rearing studies on extant relatives of ancient arthropod assemblages include published research on 28S rRNA genes of early hexapods (Dell'Ampio et al. 2009), reproductive biological and molecular investigations of Collembola (Xiong et al. 2008, Tully and Ferrière 2008), research on Hc proteins of Zygentoma (Pick et al. 2008), and improvement of phylogenetic inference using modified molecular substitution models (von Reumont et al. 2009).

    Morphological phylogenetics with focus on wing anatomy supports monophyly of the Dictyoptera, Mystroptera, and Orthopterida but higher level relationships with Dermaptera and Plecoptera are unsupported (Yoshizawa 2011).

    Stem group pterygote mayfly ichnofossils of the order Ephemeroptera are known from the Upper Carboniferous Wamsutta Formation of North America (Knecht et al. 2011).

    Permian phytophagous insects are of interest because their occurrence in deep time corresponds with early radiation of seed plants around the point in geologic time when molecular systematists tell us that the angiosperms split from the gymnosperms.

    Snakeflies (Raphidoptera) are one of the most interesting of the early divergent holometabolous insects from the evo-devo perspective but their supposed Paleozoic origins are controversial and problematic (Grimaldi and Engel 2005). Late Mesozoic baissopterid and mesoraphid snakeflies are known (J. E. Jepson et al. 2011).

    Hemimetabolous insects. Hemimetabolous, polyneopteran insects including Dermaptera (earwigs), Dictyoptera (cockroaches and termites), Grylloblattida (ice crawlers), Hemiptera (aphids and true bugs), and Orthoptera (crickets and grasshoppers) are among the most poorly understood hexapod groups from a phylogenetic perspective.

    A review of the systematics and evolution of bugs known as heteropterans is available (Weirauch and Schuh 2011).

    Important pieces of work published in the last decade are studies by Shao et al. (2003) on mitochondrial genes in hemipteroids, Fenn et al. (2008) on the mitochondrial genomes of Orthoptera, Murienne et al. (2008) on New Caledonian endemic dictyopterans assignable to Blattaria (cockroaches), Urban and Cryan (2009) on phylogenetics of Fulgoridae (lanternflies); Aristov (2010, 2011), Aristov et al. (2011), and Ren and Aristov (2011) who review the fossil history of Grylloblattida, and Perrichot et al. (2011) who report exquisitely preserved earwig nymphs from amber.

    The evo-devo of grylloblattid heads is reviewed by Wipfler et al. (2011).

    Molecular phylogenetic work on bugs includes an analysis of diaspidid nuclear, mitochondrial, and endosymbiont DNA sequences by Andersen et al. (2010) and mitochondrial 16S rRNA and nuclear 18S and 28S rRNA studies of anthocorids by Jung et al. (2010).

    A supertree of Dictyoptera, which was recently computed by R. B. Davis et al. (2009), illustrates the evolutionary success of termites (isopterans). A review of neotenous development in termites is available (Korb and Hartfelder 2008).

    The Arkhangelsk and Perm regions of western Asia and eastern Europe and Triassic beds in South Africa continue to yield fossils of extinct insect orders including the Grylloblattida (Aristov 2009 [two papers], Aristov et al. 2009, Aristov 2010, 2011).

    Triassic and Jurassic sediments of China continue to yield new species of Hemiptera assignable to Aphidomorpha (Y. Hong et al. 2009), Archaeorthoptera (J.-J. Gu et al. 2011), and Procercopidae and Tettigarctidae (B. Wang and H. Zhang 2009). Palaeontinid bugs have been found preserved in the Upper Jurassic rock record of Europe (Wang et al. 2010).

    The Upper Jurassic Morrison Formation of North America has yielded its first fossil insect, which is referable to Orthoptera (D. M. Smith et al. 2011).

    Cretaceous amber deposits in western Europe contain whole body fossils of bugs assignable to Neazoniidae (Szwedo 2009) and Pygidicranidae (Perrichot et al. 2011). Grylloids have been recovered and studied from samples of Upper Cretaceous Burmese amber (Gorochov 2010 [two papers]).

    Paleozoic origin of the Holometabola. The first essay on the Origin of Flowering Plants provided a foundation for understanding the nature and timing of early molecular diversification of homeotic selector genes, developmental proteins, nuclear receptor proteins, and cis-acting TFs of spermatophytes and arthropods.

    I also suggested that the place and time to begin a molecular phylogenetic analysis of arthropod tool kits was the DeCARB hypoxic icehouse.

    Grimaldi and Engel (2005, page 333) raise the key question, "... how did they [Holometabola] evolve" ...?

    Earlier, I painted a picture that global catastrophe might have played a role in coevolution of insects and seed plants. Molecular coevolution between arthropod and gymnosperm developmental tool kits was suggested as a way to explain evo-devo of holometabolous (larvae-forming) insects residing in crevices of bark, cones, leaves, protoflowers, and wood of shrub lifeboats in Permo-Carboniferous and Permo-Triassic compartments. Several questions may be posed with these ideas in mind:

    What did external biotic (host plant hormonal and secretory, fungal, microbial, viral) and environmental (hypercapnia, hypoxia temperature extreme) factors have to do (if anything) with evo-devo of larval moult cycles and innovative mouthpart designs of holometabolous insects such as early bees, beetles, flies, and wasps?

    Two important reviews are available on the subject of deep time coevolution of wasp parasites, hosts, and pathogenic viruses with implications on the manipulation of insect behavior and the coevolution of seed plant host and arthropod tool kits (Lovisolo et al. 2003, Grimaldi and Engel, page 427, 2005). Since molecular phylogenetic studies suggest that parasitic wasps are basal to other hymenopterans, students of the paleontology of bees and flowering plants should pay close attention to these reviews.

    Further, molecular model systems used as tools in beetle genomic research and phylogenetic studies include proteins central to development (JH esterases), diapause proteins, heat shock proteins, ultraspiracle (an ecdysone nuclear receptor protein), cuticle proteins, Hxs, genes encoding vitellogenin, and apolipophorins, among others (see review by Gómez-Zurita and Galián 2005).

    Several insect systematists studying beetle (Coleoptera) evolution are employing some genes and proteins of the insect development tool kit in their phylogenetic analyses (Gómez-Zurita and Galián 2005). Gómez-Zurita and Galián (2005) discuss the utility of molecular phylogenetic characters appearing in the entomological literature in a review paper, which is organized along the lines of Floyd and Bowman (2007) for land plants (see section below).

    Did the evolution of holometabolus insects from hemimetabolous ancestors occur as a result of developing global hypoxia as a selective force during the late DeCARB?

    What role, if any, did cross-Kingdom transposon movements play in the Paleozoic origin of the Holometabola and in evo-devo of cones and protoflowers?

    The below graphic is the same crude plot of changing oxygen levels in Earth's atmosphere over geologic time based on GEOCARB III (Berner and Kothavala 2001), and other work (Beerling and Berner 2002, Huey and Ward 2005, Ward et al. 2006), which was introduced in the first essay.

    I superimposed an evolutionary tree showing the major groups of Hexapoda listed in Table 3, above. The arthropod classification scheme is based on Grimaldi and Engel (2005).

    Three of the four insect herbivore expansion phases outlined by Labandeira (2006) are superimposed on the graph. Red symbols denote points of divergence of the Class Insecta from other invertebrates, the point when pterygote (wing-forming) insects separated from wingless orders, the point of divergence of Neoptera (wing-folders) from Pterygota, and cladogenesis of the Holometabola (larvae-forming moulting insects).


    The preceding graph is based on data from Grimaldi and Engel (Figure 4.24, page 146, 2005), with additional data added from GEOCARB III (Berner and Kothavala 2001), GEOCARBSULF (Berner 2006), and Labandeira (2006).

    Panorpida and the origin of insect pollination. Permo-Carboniferous panorpoids were the ancestors of holometabolous Antliophora (Diptera [flies] and Mecoptera [scorpionflies]). When included with the Lepidoptera (moths and butterflies), Siphonoptera (fleas), and Trichoptera (caddisflies), the dipterans and mecopterids comprise the Panorpida (Grimaldi and Engel 2005).

    According to Grimaldi and Engel (page 469, Figure 12.1, 2005) Panorpida, which are a sister group to the Hymenoptera (ants, bees, and wasps), diverged more than 290 MYA (blue symbols on the above graph), roughly coincident with the angiosperm-gymnosperm split.

    Validity of the biotic pollination coevolution hypothesis has been challenged by several cogent arguments (Gorelick 2001).

    Mesozoic evolution of holometabolous insects. The final sub-section of this chapter is a brief survey of highpoints and milestones in molecular systematic and paleontologic research on the five orders of Mesozoic holometabolous insects that eat pollen and pollinate flowering plants and gymnosperms. These insect orders are studied from molecular phylogenetic research perspectives (Longhorn et al. 2010, Ishiwata et al. 2011, among others) but results are controversial. More work is needed to include fossil calibrations.

    Based upon an analysis of preserved head and mouthparts certain scorpionflies probably fed on ovular secretions of extinct seed plant groups of the anthophyte clade (Ren et al. 2009). The study by Ren and coworkers suggests that modes of biotic coevolution of gymnosperms and pollinators were in place by the Jurassic Period of the Mesozoic Era.

    A recent review of feeding strategies and mouthpart anatomy of Mesozoic insects by Labandeira (2010) offers additional data and discussion complimenting Doug Ren's studies cited above.

    Palynivores and pollinators: the "big five." The "big five" palynivores and pollinators (page 241, Labandeira 2000) are Coleoptera, Diptera, Hymenoptera, Lepidoptera, and Thysanoptera.

    A bee pollinator is pictured to the right while visiting a cluster of flowers.

    Coleoptera. Of these five orders, the Coleoptera contain about as many species as flowering plants. Phylogenetic relationships of beetles and weevils with ancient Holometabola are a subject of continuing controversy (Longhorn et al. 2010). Major cladogenic events in the Coleoptera have been clarified by optimizing nucleotide substitution rates using Bayes factors (Pons et al. 2010).

    Expressed sequence tag databases are being used to understand the big picture in beetle molecular systematics (J. Hughes et al. 2006). Key papers by Hunt et al. (2007) and Hunt and Vogler (2008) provide a synthesis on the Mesozoic and Cenozoic superradiation of major lineages of beetles.

    Use of nuclear genes that code for alpha-spectrin, arginine kinase, CAD, enolase, PEPCK, RNA polymerase II, topoisomerase, and wingless protein show promise in deducing beetle phylogeny (Wild and Maddison 2008).

    The oldest beetle is known from the Carboniferous Period (Béthoux 2009). Late Triassic (Carnian) beetle elytrae are discussed in a recent paper by Meller et al. (2011).

    Paleobiology and fossil history of the Euaesthetinae and Steninae (Staphylinidae) is reviewed by Clarke and Chatzimanolis (2009). Novel elateriform and tenebrionoid beetles have been recovered from Jurassic sedimentary beds of Asia (Yan and B. Wang 2010, B. Wang and H. Zhang 2011). A brief account of Jurassic nemonychid (curculionoid) beetles is available (Legalov 2010).

    Tremendous progress has been made in the last decade on unraveling and better understanding complex phylogenetic relationships of beetles (Farrell 1998, and Bernhardt 1999, among many other papers). Staphylinid beetles, one of the largest groups of phytophagous coleopterans, represented by Libanoeuaesthetus (Euaesthetinae) is known from the early Cretaceous (Lefebvre et al. 2005).

    Molecular phylogenetic studies of beetles and weevils are underway in several labs including analyses of rRNA variation across 167 taxa of Chrysomelidae (Gómez-Zurita et al. 2008), comparative 18S and 28S rDNA sequence analysis of Chrysomelidae and Curculionoidea (Hundsdoerfer et al. 2009, Marvaldi et al. 2009), rRNA ITS2 sequence variation research in Meligethinae (Trizzino et al. 2009), 16S rDNA-based investigations on Thylacosterninae (Vahtera et al. 2009), nuclear gene studies of Carabidae and Trachypachidae (Maddison et al. 2009), molecular systematic investigations of staphylinids belonging to tribe Athetini (Elven et al. 2010), and combined molecular and morphological phylogenetic analyses of fungus-growing xyleborinid ambrosia beetles (Cognato et al. 2011).

    It is widely accepted that certain phytophagous insect groups diversified together with their flowering plants hosts (Wilf et al. 2000, Grimaldi and Engel 2005, Crepet and Niklas 2009). Increasingly detailed studies demonstrate that beetle and weevil diversification is out-of-sync with radiations of angiosperm families and genera (Gómez-Zurita et al. 2007, McKenna et al. 2009, McKenna 2011).

    This phenomenon is addressed by Kergoat et al. (2011) in a study of bruchid beetle co-radiation with legumes. Simply put, seed beetle lineages are much older than originally thought (Kergoat et al. 2011).

    Molecular phylogenies of chrysomelid leaf beetles suggest a younger age of the group than previously realized (Gómez-Zurita and Galián 2005, Gómez-Zurita et al. 2007). These findings contradict earlier proposals on a coevolutionary origin of angiosperms during the Cretaceous Period (Farrell 1998, Grimaldi 1999, Wilf et al. 2000, among others).

    Morphologically based phylogenies of beetles yield important clues on the timing of early macroevolutionary branching events in Coleoptera (e.g. Beutel et al. 2008, among others), and yield insight into microevolutionary insect antagonist/plant host dynamics (Borghuis et al. 2009).

    At least one milestone higher level cladistic analysis of weevils by Marvaldi (1997) was based principally on larval characters.

    Diptera. The molecular systematics and evolution of Diptera is incrementally reviewed by Wiegmann et al. (2003) and Wiegmann et al. (2011), among others. Conrad Labandeira (2005) offers one of the more complete bibliographies on the paleobiology of dipterans.

    Flies and the origin of flowering plants are discussed by Labandeira (1998) and Ren (1998). Fossilized mouthparts of brachyceran flies identified by Ren (1998) may indicate a close association with angiosperms: "... it is equally likely that basal brachyceran lineages of flies were pollinating anthophytes other than angiosperms ..." (page 58, Labandeira 1998).

    Archaic brachycerans are known from Jurassic deposits on the Indian subcontinent (Mostovski and Jarzenmbowski 2000). Research findings on the Mesozoic fossil history of brachyceran and kovalevisargid flies continues to appear in the literature (J. Zhang 2010, 2011).

    Work on the molecular systematics of flies includes studies by Bertone et al. (2008), Menguai et al. (2008), Ekrem et al. (2010), and Trautwein et al. (2010), among others.

    Hymenoptera. A study of nuclear protein coding sequences and the amino acids they encode provides strong support for Hymenoptera as sister to all other Holometabola (Ishiwata et al. 2011).

    Important insight has been recently gained on phylogenetic relationships of the megaradiation of families of ants, bees, and wasps in a studies by R. B. Davis et al. (2010) and Heraty et al. (2011). A single origin of parasitic Vespina from basal phytophagous families is suggested by molecular phylogenetic analysis of DNA sequences from four regions of hymenopteran genomes (Heraty et al. 2011).

    Diversification of angiosperms might be intertwined with early Mesozoic diversification of bees (Danforth et al. 2006). Danforth and coworkers (2006) have applied DNA sequence and morphological data toward a phylogeny of Andrenidae, Colletidae, Halictidae, and Stentrididae bees.

    Michael Engel and André Nel and coworkers continue to describe new groups of bees and wasps that provide phylogenetic insight on Hymenoptera to calibrate and/or minimum age map early branch points computed from molecular data (Michez et al. 2009, Perrichot et al. 2009, Ortega-Blanco et al. 2011, among others). African bees assignable to Anthophila are reviewed by Kuhlmann (2009).

    Genomic studies by Dearden et al. (2006) reveal that honey bees and fruit flies are the most widely diverged species of Holometabola. Apid, colletid, halictid, megachilid, melittid bee and wasp phylogenies have been computed from genetic and/or morphological data (Danforth et al. 2006, Patiny et al. 2008, Praz et al. 2008, Almeida and Danforth 2009, Cardinal et al. 2010, Rehan et al. 2010, among others).

    Papers published by Brady et al. (2006), Moreau et al. (2006), Bacci et al. (2009), and J. A. Russell et al. (2009), among other papers, are many gateways to the vast literature on the evolution of herbivory and phylogenetic relationships of ants.

    Lepidoptera. Butterflies and moths figure prominently in classic papers on coevolution and radiation of angiosperms with insects (Ehrlich and Raven 1964, Raven 1977, Labandeira et al. 1994, among others). Despite the possible importance of lepidopterans toward the explosive radiation of basal angiosperms, eudicots, monocots, rosids, and asterids, relatively little is known of phylogenetic relationships of butterfly and moth lineages in deep time (see Figure 297, page 224-225, Rasnitsyn 2002).

    A lepidopteran is visiting a flowering head of Achillea millefolium (Asteraceae, Asterales, Asteranae), which is pictured to the left.

    Milestones in ongoing research on the phylogenetic systematics of families and tribes of moths and butterflies (Lepidoptera) include studies by J. S. Miller et al. (1997), Lopez-Vaamonde et al. (2006), Regier et al. (2008), Silva-Brandão et al. (2008), Warren et al. (2008), Kawahara et al. (2009), Pohl et al. (2009), Wahlberg et al. (2009 [two papers]), and Zahiri et al. (2011), among others.

    Phylogenetic studies on butterflies and moths include published work by Lisa de-Silva et al. (2010), Kodandaramaiah et al. (2010), Mutanen et al. (2010), and Ohshima et al. (2010), among others.

    Wheat et al. (2007) revisit classical concepts in butterfly-host plant coevolution with a temporal analysis of glucosinoylate-feeding Pieridae. Another potentially interesting problem from a coevolutionary perspective is addressed by a paper published by Strutzenberger et al. (2010) having to do with shifting geometrid moth antagonists and Piperales host plant species.

    Thysanoptera. Oldest members of aeolothripids and thripids (Thysanoptera) have been reported from lower Cretaceous sediments of Transbaikal, Asia (Shmakov 2009). Early Cretaceous sediments have yielded a novel family of Thysanoptera described as Moundthripidae by P. Nel et al. (2007).

    There are many taxonomic papers in the literature on the paleoentomology of Baltic and Rovno amber deposits. Cenozoic arthropod paleobiology is beyond the scope of my essay.

    I now outline a Paleozoic and Mesozoic fossil history of the major seed plant orders necessary to understand the paleobotany of angiosperm origins. Each order is accorded chapter status in this essay. Chapters are arranged alphabetically by taxonomic order, for the Paleozoic Era and Mesozoic Era, respectively.


    Cycadales:

    A Paleozoic origin of cycads is demonstrable based on the work of T. N. Taylor (1969) but the evolutionary relationships of some early fossil forms (e.g. Phasmatocycas, Mamay 1969, 1973, 1976) is open to reinterpretation (Axsmith et al. 2003). Nilssoniales are often treated as an evolutionary branch distinct from the cycads (Krassilov 1997). I include the group here, which is in line with T. N. Taylor et al. (2009).

    There are ten extant genera of cycads, and many of the more than 300 living species are insect pollinated (Christenhusz et al. 2011).

    A living specimen of Cycas revoluta (Cycadaceae, Cycadales) is pictured to the right. The brownish fertile leaves that bear bright red seeds are termed megasporophylls. Fertile leaves and green vegetative megaphylls are produced spirally on the monopodial SAM. The SAMs of some cycads contain colonies of beetles and weevils (Norstog et al. 1986, Norstog and Fawcett 1989).

    The cycad literature is extensive covering the Carboniferous, Permian, Triassic, Jurassic, Cretaceous, and Paleogene periods (Harris 1961, T. N. Taylor 1969, Delevoryas and Hope 1976, Smoot et al. 1985, Krassilov and Bugdaeva 1988, Zhu et al. 1994, Spicer and Herman 1996, among others).

    Work appearing in print during the first decade of the 21st century includes papers by Bremer et al. (2003), Klavins et al. (2003), Archangelsky and Villar de Seoane (2004), Krassilov and Doludenko (2004), Hermsen et al. (2006), Watson and Ash (2006), Pott et al. (2007), Hermsen et al. (2009), Cúneo et al. (2010), Erdei et al. (2010), Passalia et al. (2010), and S.-J. Wang et al. (2011), among others.

    Molecular phylogenetic analyses of cycadophytes are available (Hill et al. 2003, Zgurski et al. 2008). Volume 70, Number 2 of The Botanical Review (2004), compiles some of the research on these seed plants.

    Paleozoic cycads (e.g. Crossozamia and Lasiostrobus) are hermaphroditic cycads known from both China and North America (Norstog and Nicholls 1997, L. Liu and Z. Yao 2002). In many of the known fossil plant localities, cycad fossils (with preserved reproductive structures) are found with sterile leaf fragment impressions referable to the form genus Taeniopteris.

    The Paleozoic spermopterid seed plants Archaeocycas whitei (page 8, Mamay 1976), Eophyllogonium cathayense (Mei et al. 1992), Phasmatocycas bridwellii (Axsmith et al. 2003), and Sobernheimia jonkeri (Kerp 1983) might be ovulate pieces of bisexual gigantopteroid proanthostrobili with the male parts missing. I regard all four of these species as a whole new group of gigantopteroid Paleozoic seed plants and do not include them in the Cycadales where T. N. Taylor et al. (pages 709-713, 2009) discusses them, which is in line with Axsmith et al. (2003).

    Triassic cycads have been reported (Ash 1985, Delevoryas and Hope 1971, 1976; Ash 2001, Rozynek 2008, X. Wang et al. 2009, and Molsan et al. 2011, among others) including recent Antarctic fossil finds described as Antarcticycas schopfii (Smoot et al. 1985, Hermsen et al. 2006) and Delemaya spinulosa (Klavins et al. 2003, Schwendemann et al. 2009). Hermsen et al. (2006) report on the anatomy of stems and leaves of these fossils together with a discussion of the evolution of the group.

    Jurassic cycads are well known principally of the work by Harris (1932, 1941, 1954, 1961, 1964). Harris (1961) and Tidwell (2002) are keys to the literature on the fossil history and paleobiology of cycads. Enigmatic fossils from the Jurassic Period, possibly transitional between earlier gymnosperms and later cycads include Baruligyna disticha from the Callovian of Georgia in western Asia (Krassilov and Doludenko 2004); a close relative of Semionogyna, from the Lower Cretaceous of Transbaikalia, Russia (Krassilov and Bugdaeva 1988).

    Work on Cretaceous and Paleogene cycads of the world continues (Spicer and Herman 1996, Erdei et al. 2010, Passalia et al. 2010, Shczepetov and Golovneva 2010).

    The image to the left is a male cone of Cycas revoluta (Cycadaceae, Cycadophyta) from a plant in cultivation, photographed by the author.

    Known gross morphological characters of some of cycads, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--monopodial shrubs with the main stem sheathed in helically arranged cataphylls (Smoot et al. 1985, Hermsen et al. 2006)

    REPRODUCTIVE MODULES--cones (Harris 1941, Zhu et al. (1994), Klavins et al. 2003), ovule-bearing leaves (megasporophylls) are incompletely known from compressions and impressions (Zhu et al. 1994); a bipinnate microsporophyll has been described as Androcycas santucci (Watson and Ash 2006)

    Permineralized pollen cones with pollen are described as Delemaya spinulosa (Klavins et al. 2003); additional permineralizations of reproductive material are needed to better understand pollination biology and reproductive anatomy. Is Delemaya spinulosa the male cone of Antarcticycas schopfii?

    LEAVES--cuticles (Harris 1932); simple and strap-shaped leaves which are associated with ovules have been described as Archaeocycas (Mamay 1976); Nilssoniocladus (Volynets 2010); Nilssoniopteris (Toshihiro Yamada et al. 2009); and compound pinnate leaves e.g. Zamites tidwellii (Ash 2001) are well-known from Mesozoic and Cenozoic rocks

    PHYTOPHAGOUS ASSOCIATE(S)--arthropods belonging to the Caloneurodea, Orthoptera, Protorthoptera (Beck and Labandeira 1998), insect frass not assignable to a particular species is known from permineralizations of Antarcticycas (Hermsen et al. 2006); vertebrate coprolites require discovery and study; fossilized invertebrate exoskeletons and permineralized insect guts are needed for study

    PLANT IDENTIFICATION(S)--Taeniopteris (Labandeira 1998); definitive anatomical data are needed for precise taxonomic and nomenclatural placement of the form genus into a family and genus belonging to the Cycadales

    Antarcticycas schopfii is the host plant for unknown insect phytophagous associates (Hermsen et al. 2006); important insights have been gained as summarized by Hermsen et al. (2006), but much more paleobotanical research is needed

    HOST SEED PLANT ORGAN(S) BEING EATEN--leaves (Beck and Labandeira 1998) and cataphylls (Hermsen et al. 2006), more permineralizations require discovery and study

    Numerous studies on the evolutionary relationships, genetics, molecular systematics, phytophagous insect associates, pollination ecology, and taxonomy of extant cycads are published by Stevenson (1980, 1981), Norstog et al. (1986), Norstog and Fawcett (1989), Waggoner (2001), Terry et al. (2004), P. Zhang et al. (2004), Azuma and Kono (2006), Sass et al. (2007), and Wu et al. (2007), among others.

    Additional work on cycads includes papers written by Terry et al. (2007), Cabrera-Toledo et al. (2008), S.-M. Chaw et al. (2008), D. A. Downie et al. (2008), González et al. (2008), González-Astorga et al. (2008), Rozynek (2008), Schutzman et al. (2008), R. Singh and Radha (2008), A. S. Taylor et al. (2008), Chiang et al. (2009), Lindstrom (2009), Pinares et al. (2009), Proches and Johnson (2009), Toshihiro Yamada et al. (2009), X. Wang et al. (2009), Cabrera-Toledo et al. (2010), Kyoda and Setoguchi (2010), Volynets (2010), Xiao et al. (2010), Gorelick and Olson (2011), Marler and Niklas (2011), and Olson and Gorelick (2011), among others.

    Cycads have figured prominently in classic papers on the origin of angiosperms (Arber and Parkin 1907, E. Anderson 1934, Crane 1985). Further, modern syntheses (e.g. D. E. Soltis et al. 2007) suggest that WGDs were important in the early evolution of the angiosperm stem group. Yet, "it is noteworthy that polyploidy is absent in some ancient plant lineages, such as the cycads" ... (page 376, Crepet and Niklas 2009).

    Gorelick and Olson (2011) discuss seed plant WGDs and the apparent lack of polyploidy in cycads from theoretical research perspectives of chromosomal abnormalities, heterochrony, linkage disequilibrium, reproductive isolation, and saltation.


    Gigantopterids:

    One of the missing seed plant groups in the many published phylogenetic reconstructions of seed plants is the abundant and morphologically diverse group of Carboniferous and Permian pteridosperms generically termed gigantopterids.

    Reviews by Booi et al. (2009) and DiMichele et al. (2011) support a prevailing view among paleobotanists that gigantopterids are a polyphyletic group composed of several late Paleozoic families of seed plants incertae cedis characterized by large megaphylls with reticulate venation.

    An intriguing addition to the suite of Asian and American gigantopterids is Euparyphoselis (DiMichele et al. 2011).

    Gigantopterids classified in the orders Gigantopteridales and Gigantonomiales are two of several extinct gymnosperm orders discussed in literature as possible ancestors of flowering plants (T. N. Taylor et al. 2009). Some species of gigantopterids discussed by X. Li and Yao (1983) might be peltasperms (T. N. Taylor et al. 2009, DiMichele et al. 2011).

    I lump Paleozoic spermopteroid seed plants Archaeocycas whitei (page 8, Mamay 1976), Eophyllogonium cathayense (Mei et al. 1992), Phasmatocycas bridwellii (Axsmith et al. 2003), and Sobernheimia jonkeri (Kerp 1983) with gigantopterids for now.

    Potential importance of gigantopteroid 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 term "gigantopteroid" was first adopted by Mamay et al. (1984) to pigeon-hole the youngest Permian plant megafossils known at that time.

    The reproductive anatomy, taxonomy, and evolutionary relationships of enigmatic gigantopterid seed plants is problematic (Booi et al. 2009). Presence of woody leaf midribs and cuticles on large leaves up to 30 centimeters in length (Mamay et al. 1988), and sparse reproductive material (X. Li and Z. Yao 1983), suggests that gigantopteroids are gymnospermous (T. N. Taylor et al. 2009).

    The kodachrome to the right is a nearly complete leaf of the gigantopteroid Delnortea abbottiae (USNM 364419). The image was captured on film the day the rock slab was unearthed and collected from the Lower Permian (Leonardian) Cathedral Mountain Formation.

    Little is known of the whole plant morphology of Carboniferous and Permian gigantopterids although some paleobotanists have deduced a vine habit for these gymnosperms incertae cedis (H. Li et al. 1994, H. Li and D. W. Taylor 1999). A possible connection with the enigmatic pteridosperm order Peltaspermales has been recently suggested (T. N. Taylor et al. 2009).

    The place and time to begin a survey of gigantopterids is in Cathaysian rocks of the Permian Period of China (H. Xilin et al. 1996). The Upper Paleozoic Era consists of two geologic periods: Carboniferous (Mississippian and Pennsylvanian) and Permian.

    In Paleozoic times gigantopterids were a diverse group of probably unrelated vascular plants constituting one of several terrestrial vegetation types of the biogeographic provinces of Angara, Cathaysia, and North America (Read and Mamay 1964, X. Li and Z. Yao 1982, Mamay et al. 1984).

    Gigantopterids had several morphologic features: woody midribs, erect vernation, abscission layering at the base of petioles, vessels, and libriform fibers (X. Li and Z. Yao 1983, Mamay et al. 1988, H. Li and Tian 1990, H. Li et al. 1994, H. Li et al. 1996, R. Weber 1997, H. Li and D. W. Taylor 1998, 1999), remarkably similar to characters found in bennettitaleans, gnetophytes, and certain extant flowering plants.

    Glasspool and coworkers state in a paper that defines the taxonomic concept of gigantopterid:

    "These 'angiospermous' features [leaf size and shape, organization of the stele, and presence of vessels] have led to previous evolutionary scenarios suggesting angiosperm derivation from gigantopterid origins (Asama 1982) although these are now largely discounted (e.g. Doyle 2000) and most likely represent large-scale convergence in vegetative morphology and physiology."

    The preceding statement is quoted from pages 1339 and 1340 of I. J. Glasspool, J. Hilton, M. E. Collinson, and S.-J. Wang (2004), Defining the gigantopterid concept: a reinvestigation of Gigantopteris (Megalopteris) nicotianaefolia Schenck and its taxonomic implications, Palaeontology 47(6): 1339-1361. Remarks in brackets [] are mine.

    I disagree with the opinion of Glasspool and coworkers. Simply put, detailed study of polished thin-sections of permineralized fertile gigantopterid plant material is required to justify considerations of the magnitude stated in the two papers published by Glasspool et al. (2004).

    Reproduction in gigantopterids is incompletely known (X. Li and Z. Yao 1983, R. Weber 1997). Eophyllogonium cathayense (Mei et al. 1992) bears resemblance to both gigantopteroids and taeniopteroids.

    Taxon-specific biomarkers known as oleonone triterpanes are documented from gigantopterid fragments preserved in coal ball permineralizations, and in leaf compressions (Moldowan and Jacobson 2002). Oleananes are also TSBs for angiosperms and Bennettitales. Oleonone triterpanes have been isolated from several gigantopterid leaf specimens, fossilized bennettitalean foliage, pyrolized extant angiosperm plant material, and from leaf compressions of flowering plants (D. W. Taylor et al. 2006).

    At the left is a fragment of a leaf of Taeniopteris multinervis collected from the Lower Permian (Leonardian) Cathedral Mountain Formation in the same bedding planes as Delnortea. The image of the fossil was captured by Dave Rohr. The rock specimen is deposited in the University of California Paleontology Museum (UCMP).

    Was this detached heteroblastic foliar organ part of the Delnortea plant?

    Were these seed plants forerunners of anthophytes (including flowering plants) or eudicot angiosperm analogs that diminished in numbers at the close of the Permian Period?

    Known gross morphological characters of gigantopterids, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--unknown, possibly shrub- and/or vine-like (H. Li et al. 1994, H. Li and D. W. Taylor 1999), stems possess a bifacial cambium with vessels (H. Li and D. W. Taylor 1998, 1999); additional paleontologic data are needed to reconstruct whole plants and nodal anatomy

    REPRODUCTIVE MODULES--inadequate data, possibly phyllospermous (X. Li and Z. Yao 1983, Mamay et al. 1988, R. Weber 1997), details of ovule attachment to laminar microsporophylls are needed, internal anatomy of ovules unknown, anatomy of microsporangia and pollen are unknown; anatomical and developmental details of sexual reproduction unknown, permineralizations are in need of discovery and study

    LEAVES--dicot or Gnetum-like with simple with flaring petioles and four orders of reticulate venation (Mamay et al. 1988) or Calophyllum-like (R. Weber 1997); woody midribs, and abscission zones (Mamay et al. 1988); or compound pinnate with spines, reticulate venation, waxy cuticles, sclerenchyma, secretory ducts, and certain conducting tissues. Attachment details of leaves to stems are unclear (Z.-Q. Yao and P. R. Crane 1986, H. Li and Tan 1990, H. Li et al. 1994, H. Li et al. 1996, H. Li and D. W. Taylor 1998, H. Li and D. W. Taylor 1999, Z.-Q. Wang 1999, Glasspool et al. 2004, Z.-Q. Yao and Liu 2004, Booi et al. 2009)

    The leaf marginal vein of Euparyphoselis found in both American and Asian Permian rocks is a defining feature of this genus (DiMichele et al. 2011)

    Despite the abundance of Cathaysian gigantopterid compressions and impressions summarized by X. Li and Z. Yao (1982), X. Li and Z. Yao (1983), H. Xilin et al. (1996), Z.-Q. Wang (1999), Glasspool et al. (2004), Booi et al. (2009), and DiMichele et al. (2011) study of heretofore undiscovered permineralized leaf fossils would yield more useful information

    Cuticles of Euparyphoselis reflect remarkable detail in abaxial leaf stomatal complexes, which are haplocheilic (DiMichele et al. 2011)

    PHYTOPHAGOUS ASSOCIATE(S)--arthropods belonging to the Caloneurodea, Orthoptera, Protorthoptera (Beck and Labandeira 1998); vertebrate coprolites require discovery and study, known leaf bite- and chew marks need analysis, more fossils are needed for study

    PLANT IDENTIFICATION--Cathaysiopteris, Gigantopteridium, Zeilleriopteris (Labandeira 1998); Gigantonoclea hallei, Gigantonoclea lagrelii (Glasspool et al. 2003)

    HOST SEED PLANT ORGAN(S) BEING EATEN--leaves (Beck and Labandeira 1998, Glasspool et al. 2003), permineralizations of plant tissue, tetrapod coprolites, and insect frass require discovery and study

    Are Delnortea abbottiae and Evolsonia texana gigantopteroids or gigantopterids?

    Detached pieces of taeniopteroid-type Paleozoic leaves could belong to gigantopteroid plants having dimorphic foliage, as inferred from poorly preserved compressions and impressions discussed in a progress report by X. Li and Yao (page 321, 1983), and later illustrated by X. Li and Yao (page 26 and Plate 4, 1983), Mei et al. (page 101, Plate 2, 1992), and R. Weber (page 232, Plate 3, 1997).

    Clearly, detailed studies of permineralized material of fertile gigantopteroid leaves, when unearthed, thin-sectioned, and described, would shed light on these enigmatic forms and help us to decipher their evolutionary relationships with sympatric Paleozoic congeners.

    Gigantopteroids or gigantopterids? American delnorteas and evolsonias. Permian rocks of North- and South America yield several species of gigantopterids including Cathaysiopteris yochelsonii (Mamay 1986), Delnortea abbottiae (Mamay et al. 1986), Euparyphoselis (DiMichele et al. 2011), Evolsonia texana (Mamay 1989), Gigantonoclea sp. (Mamay 1986, 1988), Gigantopteridium americanum (Koidzumi 1936), Lonesomia mexicana (R. Weber 1997), and Zeilleropteris wattii (Mamay 1986). Late Paleozoic floral zones of the Permian of the western hemisphere including Alaska (Mamay and Read 1984), though dominated at least in part, by Gigantopteridaceae, are paleofloras without Gigantopteris (Mamay et al. 1988).

    Large leaf compressions and permineralizations including a permineralized leaf midrib (see left) of Lower Permian (Leonardian) plants were described about 20 years ago (Mamay et al. 1986, 1988). Delnortea abbottiae is now known from North American and South American sedimentary beds (Ricardi et al. 1999).

    Leaves of Delnortea abbottiae are up to 30 cm long however, most of the specimens are fragmentary and the form of the whole plant is a mystery. Rock layers yielding Delnortea leaves also possessed retuse taeniopterid fragments (Mamay et al. 1984), which I now assign provisionally to Lonesomia mexicana (R. Weber 1997).

    Pictured to the left is a piece of a partially permineralized Delnortea abbottiae specimen, which was photographed before the midrib was thin-sectioned and prepared. The thin-sectioned samples of USNM 372427 are illustrated by Mamay et al. (page 1418, Figures 24-28, 1988).

    The phrase on page 760 of T. N. Taylor et al. (2009), "most specimens of D. abbottiae are 3-5 cm long," is misleading. Fewer than 20 tiny, 3-5 cm long leaves were found in the uppermost two decimeters of Section IV, Unit 5 of the Cathedral Mountains Formation just below a three meter thick layer of conglomerate representing Unit 6, which was devoid of leaf fossils but yielded a permineralized log of Dadoxylon.

    One leaf specimen yielded ovoid concretions on the distal edge of the lamina, and bite marks were seen on another fossilized leaf. Microscopic study of limonitic permineralizations of Delnortea abbottiae reveal a pattern of secondary growth from a vascular cambium; a developmental syndrome often seen in seed plants (Mamay et al. 1988).

    Mamay's suggestion that the stratigraphic occurrence of Delnortea in Upper Leonardian rocks of the Cathedral Mountain Formation may lead to a better understanding of Permian floral zones is supported by discovery of Delnortea from the Artinskian of northwestern South America (Ricardi et al. 1999).

    Interestingly, in about a dozen cases where delnorteas and evolsonias are found in Cisuralian rocks of present day southwestern North America and northwestern South America these fossilized leaves are consistently associated with detached, retuse spermopteroid megasporophylls referable to Phasmatocycas sp. and Taeniopteris multinervis (Mamay et al. 1984, Mamay 1989, Ricardi et al. 1999, DiMichele et al. 2000).

    Are the detached Delnortea and Evolsonia megaphylls and spermopteroid sporophylls part of the same gigantopteroid seed plant? If true, what is the most likely morphology of these enigmatic Permian gymnosperms?

    Following the initial report of the paleobotanical discovery (Mamay et al. 1984), and later anatomical studies of Delnortea abbottiae by Mamay et al. (1988), paleontologists elucidated "dicot-like" leaf anatomy and found vessel elements in several other Cathaysian gigantopterids (H. Li et al. 1994, H. Li et al. 1996, H. Li and D. W. Taylor 1998, H. Li and D. W. Taylor 1999).

    If the preceding analysis is proven correct by paleobotanical evidence is Euparyphoselis (DiMichele et al. 2011) a gigantopteroid with protoflowers (potentially at the base of the angiosperm line[s] of evolution), or a gigantopterid having peltaspermalean reproductive structures?

    Are the gigantopterids described by X. Li and Yao (1983) better classified in the Peltaspermales? Possibly, according to T. N. Taylor et al. (2009).

    Phasmatocycas and other spermopterids. Phasmatocycas is an emerging group of ovule-bearing taeniopteroid leaves from Carboniferous (Pennsylvanian) rocks of interior North America (Axsmith et al. 2003) once thought to be allied with the cycads (Mamay 1976). Classification of detached fossilized Phasmatocycas leaves into a specific group of gymnosperms is impossible at the present time.

    The Phasmatocycas-like Paleozoic seed plants Archaeocycas whitei (page 8, Mamay 1976), Eophyllogonium cathayense (Mei et al. 1992), Phasmatocycas bridwellii (Axsmith et al. 2003), and Sobernheimia jonkeri (Kerp 1983) might be ovulate pieces of bisexual gigantopteroid proanthostrobili with the male parts missing. I regard all four of these species as a whole new group of gigantopteroid Paleozoic seed plants, and do not include them in the Cycadales where T. N. Taylor et al. (pages 709-713, 2009) discusses them, which is in line with Axsmith et al. (2003).

    Are Phasmatocycas leaves including ovule-bearing megasporophylls and microsporangia-bearing microsporophylls, the detached remains of gigantopteroid plants with two kinds of leaves and gigantic petaloid organs attached to bisexual cone axes?

    Further, did certain detached retuse-tipped taeniopteroid leaves belong to fertile axes of gigantopterid plants having dimorphic foliage (a kind of heteroblasty), as inferred by poorly preserved compressions and impressions discussed in a progress report by X. Li and Yao (page 321, 1983) and later illustrated by X. Li and Yao (page 26 and Plate 4, 1983), Mei et al. (page 101, Plate 2, 1992), and R. Weber (page 232, Plate 3, 1997)?

    Fertile material of taeniopterids from Pennsylvanian rocks of interior North America was first described as Spermopteris (Cridland and Morris 1960). The appearance of the whole plant to which spermopterid leaves were attached is a mystery.

    Spermopterids may be detached pieces of early cycadophytes or some other unknown gymnospermous gigantopteroid shrub, tree, or vine. Critical permineralizations that unambiguously demonstrate diagnostic anatomy of cuticles, epidermal patterns (including stomatal complexes and cutin nanoridges), and ovulate position on abaxial or adaxial leaf surfaces are unknown. Therefore, taxonomic assignment of spermopterids to a specific seed plant order is unsupported by lack of fossil evidence.

    To the left is a photograph of a possible immature ectopic ovule attached to a retuse megasporophyll (or the leaf was damaged before fossilization, and the object is a "tear") that I provisionally assign to Lonesomia mexicana (R. Weber 1997) or Phasmatocycas.

    What is a taeniopterid? It is an common name which refers to often abundant Paleozoic foliage that resembles the leaves of extant Calophyllum (Clusiaceae, Theales, Dilleniidae) or Musa (Musaceae, Zingiberales, Zingiberidae).

    Fossilized leaf remains of Taeniopteris are generally not attached to a stem or rachis, thus, in at least some forms it is not known whether the fossil fragments represent pieces of simple or compound leaves, or one leaf-type of fossil plants having dimorphic leaves.

    Taeniopterid leaf compressions and impressions are common in terrestrial and deltaic sedimentary deposits of the Paleozoic. Taeniopterids often co-occur with fossilized remains of detached net-veined leaves (or leaflets) of gigantopterids, gigantopteroids, and glossopterids.

    Pictured to the right is an example of a laminar microsporophyll that I provisionally assign to Phasmatocycas. Elongate rice-shaped structures on the adaxial leaf surface may be pollen-bearing sacs. The fossil I collected is the only known microsporophyll of a gigantopteroid, and is left without a complete diagnosis of the organ and the mother plant.

    The images are 280 million year old permineralizations photographed by the author in 1982 a couple days after the fossils were excavated from the bedding plane of Unit 5 of Section IV of the uppermost Cathedral Mountain Formation, Del Norte Mountains, North America. These specimens and others are deposited in the USNM (Mamay et al. 1988). The fossilized leaf imaged to the right is actual size.

    The taeniopterid microsporophyll shown to the right (if the rice-grained lumps on the permineralization are proven to be pollen-containing sacs) could be the developmental product of MIKC-type MADS-box B genes such as expression of AP3 or PI homologs along the lines suggested by D. E. Soltis et al. (2007), but in a much older i.e. 280 million year old Paleozoic gymnosperm.

    It is unknown whether megasporophylls and microsporophylls of Lonesomia mexicana or Phasmatocycas were attached to a massive bisexual cone axis of the same plant or to separate female and male individuals.

    Paleozoic spermopterids are a relatively unknown group. In Phasmatocycas bridwellii, ovules located on the lower (abaxial) surface of leaves were attached by stalks to leaf midribs but not to the leaf edges as suggested by Cridland and Morris (1960).

    In 1983 Hans Kerp described Sobernheimia jonkeri (page 713, Figure 17.23, T. N. Taylor et al. 2009) from detached megasporophylls. Were ovule-bearing leaves of Sobernheimia jonkeri parts of enormous bisexual gigantopteroid proanthostrobili with microsporophylls and perianth segments shed and therefore, evading understanding of whole reproductive axes?

    The image to the left is the distal portion of an undescribed, retuse Phasmatocycas ovulate leaf that bears resemblance to sterile taeniopterid leaves of Lonesomia mexicana (Plate 3, Figs. 1-3, page 232, Weber 1997), which is a gigantopterid according to Professor Weber.

    The two lumps shown on this image are probably ovules. The fossils were collected from exposures of the lower Permian (Leonardian) Cathedral Mountain Formation located in the Del Norte Mountains of southwestern North America. This specimen is deposited in the USNM (Mamay et al. 1988).

    Were ovulate Phasmatocycas bridwellii leaves (Axsmith et al. 2003) detached pieces of a large bisexual cone axis, i.e. the "proanthostrobilus" (page 817, J. A. Doyle 2008) of an unknown Paleozoic gymnospermous gigantopterid tree or shrub with the pollen-bearing leaves (microsporophylls) and strap-shaped petaloid organs of the perianth missing?

    To answer this question is one of many paleobotanical challenges that require a coordinated attack strategy to be devised by developmental biologists and paleontologists.

    "... Nonetheless, it is possible that co-expression of AP3- and PI-homologs [MIKC-type MADS-box B genes, see Chapter on Genetics Considerations] mediated the evolutionary innovation of animal-attractive, petal-like organs well before the appearance of flowers."

    The preceding passage is quoted from page 361 of D. E. Soltis, H. Ma, M. W. Frohlich, P. S. Soltis, V. A. Albert, D. G. Oppenheimer, N. S. Altman, C. dePamphilis, and J. Leebens-Mack (2007), The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression. Trends in Plant Science 12(8): 358-367. The phrase in brackets [] is mine.

    Howe and Cantrill (2001) describe paleosols from the Albian of Antarctica having lenses of fossilized, detached Taeniopteris daintreei leaves, Carnoconites crantwelli ovulate organs, and Pentoxylon stems. Did these organs belong to a shrub-like Pentoxylon plant?

    Paleozoic spermopterids, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--unknown, Phasmatocycas bridwellii was possibly shrub-like (Axsmith et al. 2003); additional paleontologic data are needed to reconstruct whole plants and nodal anatomy

    REPRODUCTIVE MODULES--Phasmatocycas: the modules are phyllospermous (Cridland and Morris 1960, Mamay 1973, Axsmith et al. 2003), ovules attached to midribs on the lower (abaxial) surface of laminar megasporophylls

    Were detached sporophylls of Phasmatocycas, including the undescribed microsporophyll pictured above and sterile taeniopterid leaves (perianth parts), pieces of a massive "proanthostrobilus" sensu J. A. Doyle (page 817, 2008), which was attached to a gigantopteroid shrub having dimorphic leaves?

    The only known spermopterid male specimen (illustrated above) suggests placement of rice-grained shaped pollen sacs on the upper (adaxial) surface of the microsporophyll; anatomical and developmental details of sexual reproduction unknown, permineralizations are in need of discovery and study

    LEAVES--taeniopteroid with a stout multi-stranded midrib, the lateral veins parallel resembling Clusiaceae or Musaceae (see above), whole leaves unknown but probably simple (Cridland and Morris 1960, Mamay 1973, Axsmith et al. 2003); permineralizations with preserved leaf anatomy are needed for study

    PHYTOPHAGOUS ASSOCIATE(S)--arthropods belonging to the Caloneurodea, Orthoptera, Protorthoptera (Beck and Labandeira 1998); vertebrate coprolites require discovery and study; fossilized invertebrate exoskeletons and guts are needed for study

    PLANT IDENTIFICATION(S)--Taeniopteris (Labandeira 1998); definitive anatomical data are needed for precise taxonomic and nomenclatural placement of the form genus into a known seed plant order, family, and genus

    HOST SEED PLANT ORGAN(S) BEING EATEN--leaves (Beck and Labandeira 1998); additional fossils require discovery and study

    Asian gigantopterids. Asian gigantopterids were distinct from glossopterids, extinct Permo-Triassic seed plants whose stratigraphic distribution has been used to support Wegener's Theory of Continental Drift. In 1982 X.-G. Li and Z.-Q. Yao reviewed the work to that date on the Cathaysian flora in Asia. A compilation is available in H. Xilin et al. (1996) that summarizes research on the Permian coal floras of Jiangxi Province, China.

    The most recent review of the leaf form genera of Jambi gigantopterids is by Booi et al. (2009).

    Gigantopterids from Permian rocks of Asia were first described by Schenck as Megalopteris nicotianaefolia from poorly preserved fossil impressions (Glasspool et al. 2004). Morphotype genera indigenous to Asian Paleozoic rocks are Aculeovinea, Cathaysiopteridium, Cathaysiopteris, Cardioglossum, Euparyphoselis, Gigantonoclea, Gigantonomia, Gigantopteridium, Gigantopteris, Gigantotheca, Gothanopteris, Linophyllum, Neogigantopteridium, Palaeogoniopteris, Progigantopteris, Trinerviopteris, Vasovinea, and Zeilleropteris (H. Li et al. 1994, Booi et al. 2009, DiMichele et al. 2011).

    Fossilized connections of the leaf impressions with whole plants and reproductive structures of gigantopterids are exceedingly rare or undescribed.  Permian Gigantopteris of China unearthed and studied by X.-G. Li and Z.-Q. Yao in 1983, yield a rare glimpse of fertile material: ovules and pollen-bearing organs were attached to leaves and leaf-midribs, but the anatomy and placement of the connections is indeterminate.  A relatively recent report of reproductive structures found preserved in a bedding plane in close association with gigantopterid leaves only adds to the mystery of these plants and their gymnosperm associates (Mei et al. 1992).

    Permineralized gigantopterid foliage and stems belonging to Aculeovinea yunguiensis, Gigantonoclea guizhouensis, and Vasovinea tianii (H. Li et al. 1994, Z.-Q. Wang 1999, H. Li and D. W. Taylor 1999), possess angiosperm-like vessels and libriform fibers. Leaves of Chinese gigantopterids with waxy cuticles have been described (Z.-Q. Yao and Crane 1986).

    Based on the anatomy of vessel-containing permineralized stems H. Li et al. (1994) and H. Li and D. W. Taylor (1999) proposed that gigantopterids were vines.

    Was the twining habit and innovative vessel-containing secondary xylem of Paleozoic gigantopterids attributable to the same biomechanical properties and developmental plasticity seen in extant tropical eudicots (Ménard et al. 2009)?

    Do xylem patterns sensu Carlquist (2009) in gigantopterid leaf midribs and stems offer clues on a potential neotenous origin of angiosperms?

    In 1992 Mei et al. described Eophyllogonium cathayense, an enigmatic seed plant from the Permian of China. Seed-bearing taeniopterid leaves with reticulate venation were found in the same bedding plane as sterile gigantopterid leaves assignable to Gigantonoclea acuminatiloba and Gigantopteris dictyophylloides. Was Eophyllogonium cathayense attached to a gigantopteroid plant with dimorphic, heteroblastic leaves?

    The Paleozoic fossil Sobernheimia jonkeri (Kerp 1983; page 713, Figure 17.23, T. N. Taylor et al. 2009) might also be detached megasporophylls of a massive bisexual gigantopteroid proanthostrobilus with the microsporophylls and perianth also shed and therefore, evading a complete diagnosis of the whole fertile SAM.

    Paleobotanists are better understanding the anatomy, morphology, and systematics of Cathaysian gigantopterids, but more work is needed to elucidate relationships with the detached and fragmentary fossilized remains of other Paleozoic gymnosperms including Phasmatocycas.


    Glossopteridales:

    One of the dominant vegetation types of the southern reaches of Pangaea during the Permian Period consisted of small to large trees belonging to a group of seed ferns known as glossopterids. During the late Paleozoic mesic forests of glossopterids spread poleward. Gradual warming at the South Pole led to replacement of Glossopteris forests by stands of Dicroidium. Change in the composition of overstory trees might have altered understory shrubs and herbs possibly contributing to a decline in biodiversity of herbivorous dicynodonts (Tiffney 1992, Zavada and Mentis 1992).

    Mary E. White (1986) reviews the fossil history of glossopterids. Several morphotype genera of glossopterids circumscribe detached fossil leaves (Eretmonia, Glossotheca, and Kendostrobus, among others), isolated pollen sacs (Arberiella, Lithangium, and Polytheca), ovule-bearing leaves (e.g. Scutum), compound ovulate structures (Lidgettonia etc.), detached seeds (Pterygospermum and Stephanostoma), fossil leaves (Belemopteris, Gangamopteris, Glossopteris, and Rhabtotaenia, among others), and underground parts (Vertebraria).

    Plumstead (1973) presents an illustrated discussion of the Glossopteris flora, the paleogeography of Gondwana, and Wegener's Theory of Continental Drift. Glossopteridales and the possible relationships of glossopterids with angiosperms are discussed by Retallack and Dilcher (1981) and E. L. Taylor and T. N. Taylor (1992).

    Key articles on glossopterids are published by Rigby (1967), Surange and Maheshwari (1970), Delevoryas and Gould (1971), Maheshwari (1972), Rigby (1972), Surange and Chandra (1972, 1973, 1975), Holmes (1973), Delevoryas and Person (1975), Chandra and Surange (1976), Schopf (1976), Pant and Choudhury (1977), Gould and Delevoryas (1977), M. E. White (1978), Rigby (1978), Pant and Nautiyal (1984), Pant and Nautiyal (1984), Pant (1987), and Pigg et al. (1987).

    More recent works are Pigg (1990), Pigg and Taylor (1990), McLoughlin (1990), Rigby and Chandra (1990), Pigg and Trivett (1994), Berthelin et al. (2004), Nishida et al. (2004, 2007), Tewari (2007), Prevec et al. (2008), Cariglino et al. (2009), Decombeix et al. (2009), Rydberg (2009), E. L. Taylor and T. N. Taylor (2009), and Rydberg (2010).

    Pigg and T. N. Taylor (1993), Iannuzzi (2000), and Pigg and Nishida (2006) compile particularly complete bibliographies on the fossil history of glossopterids.

    The image to the left is a plate showing the morphology of some glossopterids. It is Figure 7 from Peter R. 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 Peter Crane.

    "Figure 7. Morphology of glossopterids. -A. Ottokaria megasporophyll and associated leaf, redrawn from Pant (1977a, fig. 10E-G), orientation of megasporophyll based on Pant and Nautiyal (1984); × 1. -B. Lidgettonia africana megasporophyll, based on Thomas (1958), Surange and Chandra (1975, text-fig. 1D), Schopf (1976, fig. 8D); × 1.5. -C. Eretmonia microsporophyll, redrawn from Surange and Chandra (1975, text-fig. 1D); × 2. -D. "Glossopteris" (?Dictyopteridium) megasporophyll in axil of vegetative leaf, redrawn from Gould and Delevoryas (1977, fig. 1d), note that details of sporophyll attachment and sporophyll orientation are uncertain, see text for discussion; × 1. -E. Glossopteris sastrii leaves borne on a shoot, based on Pant and Singh (1974, text fig. 2B-D); × 0.5. -F. Pterygospermum raniganjense platyspermic ovule based on Pant and Nautiyal 1960, text-fig. 3A); × 25. -G. Pollen grain from micropyle of P. raniganjense, redrawn from Pant and Nautiyal (1960, text-fig. 4G); × 550."

    Known gross morphological characters of glossopterids, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--trees and shrubs (Pant and Singh 1974, White 1986)

    REPRODUCTIVE MODULES--ovule-bearing leaves (megasporophylls) are of two types: those of Section Megafructi produce either stalked or sessile ovules on upper surfaces of megasporophylls known as regular leaves (Crane 1985, M. E. White 1986, E. L. Taylor and T. N. Taylor 1992). In Microfructi, the ovules are attached to scale-leaves termed microphylls (M. E. White 1986)

    Ovules of Glossopteris have been described as Homevaleia gouldii (Nishida et al. 2007). Preserved sperm, pollen tubes, and ovules provide evidence of zooidogamy in Glossopteris (Nishida et al. 2003, Nishida et al. 2004)

    Gondwanan beds have yielded ovulate fructifications assignable to Arberia (Rigby 1972). Ovuliferous fructifications have been restudied and placed in Bifariala (Prevec et al. 2008)

    Pollen-bearing (male) organs of glossopterids are attached to the upper surfaces of scales described as Eretmonia, Glossotheca, and Squamella (M. E. White 1986). All three form genera display Arberiella microsporangia that produce pollen (M. E. White 1986). Fossilized peltate discs bearing taeniate pollen have been described from the late Permian of Australia by Rigby and Chandra (1990)

    LEAVES--simple, lanceolate, of the Glossopteris and Gangamopteris-type (Crane 1985, White 1986, Tewari 2007)

    PHYTOPHAGOUS ASSOCIATE(S)--wood-boring Coleoptera (Zavada and Mentis 1992, Weaver et al. 1997, Labandeira 1998). Caloneurids, orthopterans, and protorthopterans are external leaf-feeders on Glossopteris foliage (Labandeira 1998). Hypoperlids and grylloblattids feed on pollen inside of Protohaploxypinus microsporangia (Labandeira 1998)

    PLANT IDENTIFICATION(S)--Glossopteris, Protohaploxypinus

    HOST SEED PLANT ORGAN(S) BEING EATEN--bark, leaves, microsporangia, pollen, and wood

    Some workers suggest that surviving lineages of Paleozoic glossopterids are represented in Mesozoic floras by corystosperms and even Caytoniales. Thomas N. Taylor et al. (page 598, 2009) offer the most up-to-date review of glossopterids.


    Gnetales:

    The Gnetales is one of the orders of Paleozoic seed plants widely regarded as a sister group to the flowering plants (Arber and Parkin 1907, J. A. Doyle and Donoghue 1986, Cornet 1996, Krassilov 1997, J. A. Doyle 2006). There are more than 80 species of living gnetophytes representing three genera (Christenhusz et al. 2011).

    Based on molecular phylogenetic studies, a close relationship of conifers with Gnetales is supported (Y.-L. Qiu et al. 1999, Winter et al. 1999, Magallón and Sanderson 2002, Burleigh and Mathews 2004, Braukmann et al. 2009, among others). Gnetales continue to pose a challenge in many phylogenetic analyses of flowering plants and their unknown seed plant ancestors and congeners (Sean W. Graham and Ihles 2009).

    The anthophyte hypothesis was rejected by Donoghue and J. A. Doyle in 2000. Seemingly, Rothwell et al. (2009) are in disagreement with Michael Donoghue and James Doyle.

    Cones identifiable to Gnetales are well documented from Permian rocks (Z.-Q. Wang 2004) despite J. A. Doyle's assertion that "Gnetales and angiosperms are not known until the Mesozoic-late Triassic for probable stem relatives of Gnetales ..." (page 818, J. A. Doyle 2008).

    Details of the fossil history of the group are summarized by Crane (1996), Rydin et al. (2004), Z.-Q. Wang (2004), Rydin et al. (2006), T. N. Taylor et al. (2009), Tekleva and Krassilov (2009), Smirnova (2010), and X. Wang and S-L. Zheng (2010), among others.

    The main body of research on the evolutionary relationships, biology, phylogeny, and reproductive biology of the Gnetales is published in several papers by Carlquist (1996), Carmichael and Friedman (1995, 1996, 1998), Crane (1996), J. A. Doyle (1996), Endress (1996), Friedman (1996, 1998), Friedman and Carmichael (1996), Hufford (1996), Price (1996), Krassilov (2009), and Krassilov and Schrank (2011), among others.

    Debates on competing hypotheses linking gnetophytes with angiosperms are reviewed by Friis et al. (2007), Krassilov (2009), and Rothwell et al. (2009). Paleobotanical evidence (Z.-Q. Wang 2004) and molecular phylogenetic studies reviewed by Braukmann et al. (2009) support the prevailing gnepine hypothesis.

    Another lab (page 209, Rydin et al. 2002) illuminates discrepancies between the gnepine hypothesis and findings derived from studies of anatomy, morphology and paleobotany of conifers and gnetophytes constituting " ... the main impediment for reaching a consensus on seed plant phylogeny."

    Once long-branch attraction artifacts are removed the gnepine hypothesis enjoys support based on recent phylogenetic reanalysis of cpDNA sequences (Zhong et al. 2010).

    Though unstudied from the research perspective of phylogenetics, the late Paleozoic fossil Palaeognetaleana (Z.-Q. Wang 2004) adds a whole new dimension to the gnepine hypothesis and relationships of Gnetales with walchian conifers and spermopterids at the time of the MRCA.

    The image to the right is an attached fossil flower-like organ of Eoantha zerikhinii, an anthophytic gnetalean from the Baisian Assemblage, early Cretaceous Period, Transbaikalia, Russia. Four ovuliphores are visible together with a perianth of linear bracts. Each ovule contain a pollen chamber filled with Ephedrites-type pollen (this picture is from an original image provided by Professor Valentin Krassilov, posted here with his permission).

    Known gross morphological characters of Gnetales, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--shrubs and small trees (Krassilov 1997)

    REPRODUCTIVE MODULES--cupulate pre-flowers (Krassilov 1997); flower-like parts arranged in a compound cone with whorled, partially fused microsporophylls; or one or more ovules surrounded by enveloping bracts (Stewart and Rothwell 1993), reduced ovuliphores in male strobili function as nectar-producing organs (Krassilov 1997). Ovules are borne on the tips of stems; each ovule is enclosed by a bracteole. Ovules are enclosed by a fused integument and nucellus. The micropyle is biseriate and tubular. Ingrowths of cells close the micropyle and a pollen chamber are present (Rothwell et al. 2009)

    LEAVES--linear and flattened in Drewria, "dicot"-like in Gnetum, strap-like in Welwitschia, or reduced to scales in Ephedra (Stewart and Rothwell 1993). Leaves are opposite and not pinnate (Rothwell et al. 2009)

    PHYTOPHAGOUS ASSOCIATE(S)--Spathoxyela, a xyelid sawfly (see Dmitriev and Ponomarenko 2002)

    PLANT IDENTIFICATION(S)--Baisianthus (see Dmitriev and Ponomarenko 2002)

    HOST SEED PLANT ORGAN(S) BEING EATEN--pollen-bearing flower-like organs of Baisianthus (see Dmitriev and Ponomarenko 2002)

    Some of the research on the anatomy, ecology, evo-devo, fossil history, and molecular systematics of gnetophytes is published by Van Konijnenburg-Van Cittert (1992), Osborn et al. (1993), J. A. Doyle (1998), Pham and Sinha (2003), Rydin et al. (2002), Mundry and Stützel (2004), Won and Renner (2005), Hajibabaei et al. (2006), Rydin et al. (2006), Friis et al. (2007), C.-S. Wu et al. (2007), H.-M. Liu et al. (2008), McCoy et al. (2008), T. Yamada et al. (2008), X. Wang and S-L. Zheng (2010), and Kunzmann et al. (2011), among others.

    Papers of potential evolutionary and phylogenetic significance to the early divergence of Coniferales and Gnetales from the MRCA are Braukmann et al. (2009), Friis et al. (2009), S.-X. Guo et al. (2009), Hollander and Vander Wall (2009), Krassilov (2009), Kunzmann et al. (2009), Rydin and Korall (2009), Tekleva and Krassilov (2009), C.-S. Wu et al. (2009), Rydin and Friis (2010), Rydin et al. (2010), Flores-Rentería et al. (2011), and Rudall et al. (2011), among others.

    The most reduced cpDNAs are known from extant Gnetales specifically Ephedra equisetina, Gnetum parvifolium, and Welwitschia mirabilis (C.-S. Wu et al. 2009).


    Vojnovskyales:

    In Carboniferous and Permian times another intriguing group of shrub-like seed plants with palm-like leaves, leafy short shoots, and bisexual cone axes appears in the stratigraphic column (Krassilov and Burago 1981, Rothwell et al. 1996, Naugolnykh 2001). Several species have been described from Permian rocks all over the world. Perhaps the best known species are Sergeia neubergii (Rothwell et al. 1996) and Vojnovskya paradoxa (Mamay 1976).

    Vojnovskyaleans bear close resemblance in many details of leaf, reproductive, and stem anatomy to Triassic Sanmiguelia and the later pentoxylaleans (Crane 1985, Krassilov 1997, Naugolnykh 2001).

    Mamay (page 295, 1976) provoked interesting speculation on Maekawa's 1962 proposal casting Vojnovskya as a "presumable ancestor of angiosperms." It is equally interesting that some workers have drawn a connection between foliar material of Vojnovskya paradoxa and Sanmiguelia lewisii (page 779, Crane 1985).

    Another view held by Mamay is that the Vojnovskyales might be remotely related to the Bennettitales or Cordaitales, or represent "some bizarre, short-lived group of late Paleozoic gymnosperms that attained a sparse but geographically broad distribution" (page 295, Mamay 1976).

    Were the bisexual strobili of Vojnovskyales protoflowers? If so, why have so many botanists omitted these gymnosperms from seed plant phylogenies?

    Several groups of vojnovskyaleans had architectural adaptations possibly exploited by Paleozoic insects. Intriguing fossilized evidence in Paleozoic rocks of whole plant organs of Sergeia neuburgii (Vojnovskyaceae, Vojnovskyales) is published on page 1072 of Rothwell et al. (1996). Unfortunately these fossils cannot be easily screened for invertebrate remains possibly intercalated between the helically arranged leaf permineralizations, because the fossil was transported with other turbidites some distance from the shoreline (Rothwell et al. 1996).

    The image to the left consists of four drawings showing the fructification morphology of certain vojnovskyaleans. It is Figure 1 from S. V. Naugolnykh (2001), Morphology and systematics of representatives of Vojnovskyales, Paleontological Journal 35(5): 545-556, reprinted with written permission of Pleiades Publishing, Inc. I thank Serge V. Naugolnykh and the Paleontological Journal for this contribution.

    "Figure 1. Fructification morphology of representatives of Vojnovskyales: (a, c, d) Paravojnovskya (al. Gaussia) imbricata (Naug.) Naug. et Doweld, (a) specimen no. 3773(11)/326(92), (c, d) the specimen from the collection by Vaulev (Perm Regional Museum), (b) proposed arrangement of fructifications of P. imbricata on a fertile shoot, in axils of scale-form bracts of Nephropsis (Sulcinephropsis). The locality of Chekarda-1, the Kungurian, Lower Permian of the Middle Fore-Urals. Scale bar is 1 cm."

    Known gross morphological characters of Vojnovskyales, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--possibly shrub-like (Mamay 1975, 1976) with scaly, bracetose, and leafy short shoots often fertile in the developing SAMs (Krassilov 1997). Permineralizations are needed to better understand the anatomy of short shoots

    REPRODUCTIVE MODULES--globose head-like bisexual strobilus (e.g. Gaussia, Krassilov 1997) composed of basally attached ovule-bearing leaves (megasporophylls) and terminal microsporophylls each with two microsporangia attached to the distal end of each leaf; the fossils are incompletely known from compressions and impressions (Mamay 1976, Krassilov 1997). Shortened, bracteose, cone-like structures subtended by umbrella-shaped leaves that contain either pollen or stalked seeds were described by Naugolnykh (2001)

    LEAVES--simple and flabelliform in Sandrewia texana (Mamay 1975, 1976), and lanceolate in other genera (Krassilov 1997); the leaves of Permian Vojnovskya paradoxa resemble Sanmiguelia lewisii, a Triassic plant

    PHYTOPHAGOUS ASSOCIATE(S)--unknown; existing specimens should be restudied for the presence of insect remains and traces

    PLANT IDENTIFICATION(S)--not applicable

    HOST SEED PLANT ORGAN(S) BEING EATEN--not applicable

    The reproductive biology of the Vojnovskyales is not clearly understood, but some research progress has been made (Rothwell et al. 1996, Naugolnykh 2001). Additional discoveries of permineralized sexual structures are needed to better understand these seed plants and to reanalyze them in a phylogenetic context.

    "Since conifers extend back to the Late Carboniferous, this implies that the line leading to angiosperms goes back this far too - an apparent conflict with the stratigraphic record (Axsmith et al., 1998; Doyle 1998a)."

    This preceding passage is quoted from page 172 of J. A. Doyle (2001), Significance of molecular phylogenetic analyses for paleobotanical investigations on the origin of angiosperms, The Palaeobotanist 50: 167-188.


    Seed Plants of the Mesozoic Era:

    One approach toward our better understanding of flowering plant cladogenesis from the lineage(s) containing gymnospermous seed plant ancestors is to list the known fossil seed plant groups of the Mesozoic Era and to compare and contrast them with respect to morphological characters most often associated with angiosperms.

    The image to the right is a drawing of a detached spherical ovule-bearing Vardekloeftia sulcata head with densely packed ovules and interseminal scales, from a bennettitalean bush. It is Figure 9B from Peter R. 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 Peter Crane.

    "Figure 9. Morphology of the Vardekloeftia and Bennetticarpus plants. -B. V. sulcata, spherical head composed of ovules and interseminal scales, based on Harris (1932b, pl. 15, fig. 1, pl. 17, figs. 1, 2, pl. 18); × 2."

    Did sauropods and smaller herbivorous reptiles feed on these fleshy Vardekloeftia seed heads? Were the ovules and scales of this plant filled with antiherbivory poisons such as polyacetylenes and toxic cycasins?

    "In sum, from the plant's point of view, the age of dinosaurs was not an extension of Permian herbivory, nor a duplication of the present. While smaller herbivores duplicated some aspects of the preceding and following time, the immense herbivores imposed a unique selective force on the physiognomy and life history strategies of Mesozoic plants. Initially, these forces were met by a limited diversity of genetic lineages of plants, but by the end of the Mesozoic, gymnosperms with efficient vegetative growth and abilities to recover from damage (= angiosperms) had evolved. Much of the morphology and biology of Mesozoic plants should be considered in the light of this substantial herbivore pressure."

    The preceding quotation is from page 94 of Tiffney (1992), The role of vertebrate herbivory in the evolution of land plants, The Palaeobotanist 41: 87-97.

    The first occurrence of angiosperm-like palynomorphs in the stratigraphic record is from the early Triassic Period (Hochuli and Feist-Burkhardt 2004), but the anatomy and morphology of the seed plant(s) which shed such pollen is a mystery. Fossilized remains of Triassic seed plants which have flowering plant characteristics are very rare and often poorly preserved.

    I now present a brief survey of several enigmatic and sometimes spectacular seed plant finds from Triassic, Jurassic, and Cretaceous rocks.

    Sanmiguelia. Of all the enigmatic seed plants of the early Mesozoic Era, Sanmiguelia lewisii has attracted the most attention by paleobotanists. This rather common Triassic fossil of southwestern North America is remarkably similar to the Paleozoic Vojnovskyales (page 779, Crane 1985), another group of angiosperm-like seed plants from Asiatic and North American Paleozoic rocks (Mamay 1976).

    Sanmiguelia lewisii is an innovative Triassic plant having palm-like leaves (Brown 1956, Ash 1976) with flowers and angiosperm-like reproductive modules not unlike the monocotyledonous angiosperm Veratrum (Cornet 1986, 1989). Detailed studies of the reproductive morphology of Sanmiguelia have been published (Cornet 1989). Additional permineralized fossil material of Sanmiguelia is probably needed to better understand the anatomy of reproduction and whole plant morphology.

    Morphological details of Sanmiguelia, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--Sanmiguelia lewisii was a woody herb (Cornet 1986, 1989), or small shrub. Better preserved fossilized material and more anatomical data are needed to better understand the anatomy and morphology of whole plants in relation to Vojnovskyales and the angiosperms Joinvillea and Veratrum

    REPRODUCTIVE MODULES--ovuliferous inflorescences (first described as Axelrodia burgeri), polleniferous inflorescences (named Synangispadixis tidwellii), flowers with ovuliferous units and polleniferous units, megasporophylls as carpels, synangia as anthers, bracts, bitegmic ovules (Cornet 1986, 1989)

    The reproductive biology of Sanmiguelia is not clearly understood, but some research progress has been made (Cornet 1986, 1989). Additional discoveries of permineralized sexual structures are needed to better understand the evolutionary position of these seed plants in relation to other anthophytes (including monocotyledonous flowering plants) and older vojnovskyaleans

    LEAVES--simple, alternate, clasping and flabelliform to lanceolate resembling extant Veratrum californicum (Liliaceae, Liliales, Liliidae) (Cornet 1989)

    PHYTOPHAGOUS ASSOCIATE(S)--bite marks and trails of anther debris left by unknown insects (Cornet 1989); additional specimens await discovery to be studied for the presence of insect remains and traces

    PLANT IDENTIFICATION(S)--Sanmiguelia lewisii (Cornet 1989)

    HOST SEED PLANT ORGAN(S) BEING EATEN--leaf tissue and pollen? (Cornet 1989)

    Enigmatic seed plants of the Mesozoic. The early Mesozoic fossil record of seed plants is extremely sparse and poorly known. Too few paleobotanists specialize in Triassic and Jurassic paleobotany, and inadequate resources are applied toward finding early Mesozoic insect and plant fossil transitional series.

    Several enigmatic genera are known from Mesozoic rocks. These poorly known fossil forms include Baisia (Krassilov 1997), Cycandra (pollen cones resembling fossil cycads or Nilssoniales), cupules of Dirhopalostachys (reminiscent of basal flowering plants such as Lesqueria elocata), Doylea tetrahedrasperma (a corystospermous cupule or carpel-like organ, Stockey and Rothwell 2009), Fraxinopsis (Axsmith et al. 1997), Furcula (Harris 1932), Irania (with both androclades and gynoclades), Leptostrobus (a czekanowskialean with stigmatic cupules), Pannaulika triassica (Cornet 1993), and Raunsgaardispermum lusitanicum (palynomorphs resembling Bennettitales and Gnetales) (Mendes et al. 2008).

    Some recent discoveries include Schmeissneria, an intriguing seed plant incertae cedis from the earliest Jurassic Era (Lias interval) of Europe and Middle Jurassic of Asia (X. Wang et al. 2007, X. Wang 2010) and Xingxueanthus sinensis, an angiosperm-like inflorescence from the Middle Jurassic of Asia (X. Wang and S. Wang 2010).

    Jurassic Vladimariales (Gordenko 2010) are probably allied to the Ginkgoales, which are left out of the discussion for now.

    Bennettitales. By Triassic time, an intriguing group of monopodial seed plant shrubs, known as cycadeoids appears in the stratigraphic column (Crepet 1972, Crepet 1974, Crane 1986, Stewart and Rothwell 1993, Nishida 1994, Barbacka 2000, Rothwell et al. 2009, T. N. Taylor et al. 2009). These shrubs were cycad or palm-like in overall aspect. Reproductive structures were borne on modified leaves, clustered in flower-like strobili. Classified in the taxonomic order Bennettitales, cycadeoids were thought by Arber and Parkin (1907) as likely candidates as ancestors of modern flowering plants (pages 739-740, T. N. Taylor et al. 2009).

    Paleobotanists Crepet, Rothwell, and Stockey review the anatomy and morphology of the Bennettitales (Rothwell et al. 2009). The book chapter by Crepet and Stevenson (2010) is a critical library resource on Bennettitales.

    There are two or three main groups of cycadeoids often treated at the family level in the taxonomic hierarchy. Cycadeoidaceae studied by Wieland and Delevoryas include Cycadeoidea, fossilized remains of squat, shrub-like trunks bearing leaves, cones, and pollen recovered from Cretaceous rocks of North America and Monanthesia (see Delevoryas 1962). The other group classified in the Williamsoniaceae includes Williamsonia sewardiana, described from the Jurassic period of India.

    Detailed studies of bennettitaleans by paleobotanists have been underway for several decades. This work includes Bose (1968), Delevoryas (1968), Harris (1969), Crepet and Delevoryas (1972), Crepet (1972, 1974), T. N. Taylor (1973), Harris (1974), Sharma (1974, 1976, 1977), Crane (1986), Pedersen et al. (1989), Delevoryas (1991), Nishida (1994), Osborn and Taylor (1995), Saiki and Yoshida (1999), Barbacka (2000), G. Sun et al. (page 165, 2001), Rothwell and Stockey (2002), Stockey and Rothwell (2003), Watson and Lydon (2004), Boyd (2004), Friis et al. (2007), Pott et al. (2007 [two papers]), Going et al. (2007), and Y.-D. Wang et al. (2008), among others.

    Articles pertaining to cycadeoids in the scientific literature are by Crane and Herendeen (2009), Pott and McLoughlin (2009), Rothwell et al. (2009), Yamada (2009), Zavialova et al. (2009), Cúneo et al. (2010), Gordenko and Broushkin (2010), Jud et al. (2010), Osborn et al. (2010), Rothwell and Stockey (2010), and Molsan et al. (2011), among others.

    Bennettitaleans probably survived the K-T asteroid impact as evidenced by finds of putative Ptilophyllum leaf compressions in Oligocene rocks of Tasmania (McLoughlin et al. 2011).

    Some of the morphotype genera representing detached fossilized organs of bennettitaleans include Anomozamites (leaves), Bucklandia (stems and leaf bases), Cycadeoidea (branches, cones, leaves, synangia, and trunks), Cycadeoidella (Nishida 1994), Cycadolepis (cone bracts and scales, Crane and Herendeen 2009), Dictyozamites (leaves), Exesipollenites (pollen), Ischnophyton (stems and fronds), Neozamites (leaves), Nilssoniopteris vittata (leaves, Crane and Herendeen 2009), Otozamites (leaves), Pseudocycas (leaves), Pterophyllum (leaves), Ptilophyllum (leaves), Rehezamites (leaves), Tyrmia (leaves), Weltrichia (pollen cones), Williamsonia (ovulate cones), and Zamites (leaves).

    The plate reproduced on the left shows reconstructed detached organs of bennettitaleans. It is Figure 11 from Peter R. 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 Peter Crane.

    "Figure 11. Morphology of Bennettitales. -A. Williamsonia coronata, longitudinal half-section through 'flower,' based on Harris (1944, fig. 1); × 3. -B. Nilssoniopteris vittata, redrawn from Harris (1969, fig. 32A), an unusual specimen showing two lateral pinnae at the base; × 1. -C. N. vittata, detail of stoma showing paracytic guard cells and sinuous anticlinal flanges, based on Harris (1969, fig. 32D); × 1,000. -D. W. coronata, surface of immature 'gynoecium' showing micropyles and interseminal scales, based on Harris (1969, fig. 62F); × 50. -E. Cycadeoidea sp., longitudinal half section through 'flower,' based on Wieland (1906, fig. 88) and Crepet (1974, pl. 61, fig. 21); × 1.5."

    Several potentially interesting points of discussion on the assumed relationship of phytophagous insect associates with cycadeioids may be found in Crepet (1974) and T. N. Taylor et al. (page 732 and 741, 2009).

    "It is possible that predation pressure was not only responsible for the phylogenetic 'closing' of the microsporophylls, but was also responsible for the position of the cones on the trunks of Cycadeoidea which offers additional protection."

    The above quotation is from page 160 of Crepet (1974), "Investigations of the North American cycadeoids: the reproductive biology of Cycadeoidea," Palaeontographica Abt. B: 148.

    Known gross morphological characters of bennettitaleans and a list of phytophagous animal associates, references, and future research needs, are summarized below.

    WHOLE PLANT MORPHOLOGY--shrubs (Crepet 1974, Rothwell et al. 2009)

    REPRODUCTIVE MODULES--simple cones with helically arranged bracts, ovule-bearing leaves (megasporophylls), interseminal scales, and pollen-bearing leaves (microsporophylls). Nectar glands, ovules, pollen, and seeds are present. Ovules are born on the distal ends of megasporophylls. The nucellus is free from the integument and a tubular micropyle is absent. A pollen chamber is absent and the micropyle is closed by a nucellar plug (Rothwell et al. 2009)

    Fragments of Williamsoniella coronata consist of ovulate parts (with monosulcate pollen adhering to some surfaces), fragments of pollen-producing organs, scale leaves, and interseminal scales of a larger bisexual structure (Crane and Herendeen 2009)

    LEAVES--simple and strap-shaped or compound pinnate and palm-like (Boyd 2000, G. Sun et al., pages 188-190, 2001), xeromorphic with thick cuticles (Villar de Seoane 2001)

    PHYTOPHAGOUS ASSOCIATE(S)--oribatid mites, indeterminate beetles, helid and nemonychid weevils, possible pollinating parandrexid or protoceline chrysomelid beetles, unidentified nectar-feeders, and insect eggs (Crepet 1974, Dmitriev and Ponomarenko 2002, Pott et al. 2008, Jud et al. 2010)

    PLANT IDENTIFICATION(S)--bisexual fructifications of Cycadeoidea with burrows (mines), insect traces in various Mesozoic fructifications (Crepet 1974, Dmitriev and Ponomarenko 2002)

    HOST SEED PLANT ORGAN(S) BEING EATEN--leaf tissues, ovules, and pollen?

    Were peculiar modifications of female and male bennettitalean organs, specifically hairs and scales, able to deliver toxic alkaloid and polyacetylene toxins to potential vertebrate herbivores? Did extinct cycadeoids possess these antiherbivory chemical warfare agents?

    Caytoniales. The enigmatic pteridosperm order Caytoniales first appeared in the Triassic Period. By Jurassic and Cretaceous time, caytonialeans comprised a minor but important floristic element indigenous to terrestrial biomes on the northern landmasses (Krassilov 1977, 1997).

    Caytonia is a sister group to angiosperms in many emerging phylogenetic reconstructions (D. E. Soltis et al. 2005, J. A. Doyle 2006, J. A. Doyle 2008, Sean W. Graham and Iles 2009).

    Despite pivotal discussions on Caytoniales and problematic ideas on origin of the angiosperm carpel (Thomas 1925, Harris 1940, Harris 1951, J. A. Doyle 1978, J. A. Doyle 2006), the group is one of the least known of Mesozoic seed plant clades (Stockey and Rothwell 2009, T. N. Taylor et al. 2009).

    In yet another bizarre twist some paleobotanists have drawn a possible evolutionary connection between Leptostrobus (Czekanowskiales) and Irania with Caytoniales (X.-Q. Liu et al. 2006).

    A glaring absence of a fossilized Caytonia proanthostrobilus and discernable transformational series linking caytonias with basal angiosperms renders the group useless from a morphological phylogenetic perspective, in my opinion. It is unlikely that the order Caytoniales has any bearing whatsoever on the origin of flowering plants.

    Further, traditional ideas on supposed relationships of Caytonia with flowering plants are also questioned by provocative paleobotanical studies (Xin Wang 2010).

    There is no convincing paleobotanical evidence for past elegant proposals on the evo-devo of the angiosperm outer ovular integument and carpels from cupules and axillary organs of Mesozoic Caytoniales to be found in the fast moving literature on molecular tool kits and ovular TFs (Kelley et al. 2009, Skinner and Gasser 2009, R. H. Brown et al. 2010, Tavares et al. 2010).

    Simply put, cone and floral tool kits are too conserved i.e. demonstrably Permo-Carboniferous in origin to somehow accommodate bizarre morphologies seen in Mesozoic Caytoniales. Further, there is simply no evidence of a transitional series or chronocline leading from Caytoniales to the Amborellanae, Austrobaileyanae, Nymphaeanae, and Magnolianae.

    The image to the right and the figure legend below in quotation marks is from page 753 of Peter R. 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 Peter Crane.

    "Figure 17. Morphology of the Caytonia plant. -A. Sagenopteris colpodes, based on Thomas (1925, pl. 15, fig. 50); × 0.75.

    -B. S. colpodes, detail of leaflet attachment and venation, based on Harris (1964, fig. 2H); × 4.

    -C. Caytonanthus arberi, based on Harris (1941, pl. 2, fig. 3); × 7.

    -D. Pollen from C. arberi, based on Townrow (1962b, fig. 3d, e); × 1,200.

    -E. Caytonia nathorstii megasporophyll, based on Harris (1964, fig. 10-A-C); × 5.

    -F. Caytonia "cupule" containing seeds, based on Reymanowna (1973, particularly text fig. 12E, F); × 12.5.

    -G. Caytonia "cupule," longitudinal section, based on Reymanowna (1973, particularly text fig. 12E, F); × 12.5.

    -H. C. nathorstii ovule longitudinal section, redrawn from Harris (1958, fig. 7); × 110."

    Several form genera were described by Harris (1940, 1941, 1951, 1964, 1971), including Amphorispermum (seeds), Caytonanthus (pollen-bearing organs), Caytonia (cupules), Ktalenia (cupules), Sagenopteris (leaves), and Vitreisporites (pollen). Barbacka and Bóka (2000) and others provide additional details.

    General evolutionary relationships of caytonialeans with other seed plant groups are discussed by Thomas (1925), Harris (1940, 1951), Krassilov (1997), J. A. Doyle (2006), Stockey and Rothwell (2009), and E. L. Taylor and T. N. Taylor (2009), among others. Krassilov (1997) draws a possible evolutionary connection between caytonialeans and ranunculid flowering plants. Detailed discussion of the morphology and anatomy of this group of anthophytes, homology of characters, phylogenetic relationships with other seed plants, and the origin of angiosperms may be found in Krassilov (1977) and J. A. Doyle (2006), among others.

    Further, T. N. Taylor et al. (page 637, 2009) illuminate similarities between the cupules of Petriellaea (Petriellales) and Caytonia.

    Xin Wang, in a controversial paleobotanical investigation (2010), suggests that cupule bearing organs of Paracaytonia hongtaoi (Caytoniales) are parts of branches and not ovule bearing leaves.

    How is it possible that Mesozoic Caytoniales are basal to stem group flowering plants, assuming calibrated relaxed clock methods (Magallón 2010, Stephen A. Smith et al. 2010) are more precise than other approaches while taking into account putative Paleozoic divergence(s) of angiosperms from the MRCA?

    Known gross morphological characters of the Caytoniales, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--possibly shrub-like (Reymanowna 1974, Krassilov 1997). Coalifications, compressions, permineralizations, and petrifactions are needed to elucidate the form of whole plants

    REPRODUCTIVE MODULES--cupules, eight to 30 bitegmic ovules per cupule, and saccate pollen

    The reproductive biology of caytonialeans is not clearly understood, but some research progress has been made (Krassilov 1997). Additional discoveries of permineralized sexual structures are needed to better understand these seed plants

    LEAVES--compound palmate, the pinnae are lanceolate and glossopteroid in general aspect; leaves have been classified in the form genus Sagenopteris (Krassilov 1997) and later studied by Barbacka and Bóka (2000)

    PHYTOPHAGOUS ASSOCIATE(S)--indeterminate insect traces on foliage (Dmitriev and Ponomarenko 2002)

    PLANT IDENTIFICATION(S)--Sagenopteris

    HOST SEED PLANT ORGAN(S) BEING EATEN--leaves (Dmitriev and Ponomarenko 2002)

    Corystospermales. Corystosperms were once a dominant forest vegetation type of Gondwana including south polar floras (Bomfleur and Kerp 2010). The Dicroidium flora probably replaced the Glossopteris flora of the southern latitudes (M. E. White 1986) while many glossopterid populations probably declined following the EPE. The Corystospermales represented by the Paleogene Tasmanian fossil Komlopteris cenozoicus, is the only group of seed ferns that survived the K-T asteroid impact (McLoughlin et al. 2008).

    The pteridosperm order Corystospermales is receiving more interest based upon recovery of permineralized reproductive material from Antarctica, the Middle East, and North America, including, for example, preserved pollen organs described as Pteruchus; cupules, pollen, and other detached remains (Pigg et al. 1993, Osborn and Taylor 1993, Yao et al. 1995, Axsmith et al. 2000, Kerp et al. 2006, T. N. Taylor et al. 2009, among others). Compression fossils of ovulate axes described as Umkomasia are known from late Permian beds in India (S. K. Chandra et al. 2008), the Triassic Molteno Formation of South Africa (Axsmith et al. 2000), Upper Triassic of northern Asia (Shuqin et al. 2008), and from Jurassic deposits studied by others.

    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).

    Several form genera of corystosperms are known including Alisporites (pollen), Dicroidium (foliage), among other leaf morphotypes; Karibacarpon (detached ovules), Pilophorosperma (ovules and associated leaves), Pteroma (ovulate organs), Pteruchus (pollen organs and associated leaves), Rhexoxylon (permineralized wood), and Spermatocodon (ovulate organs).

    The image to the left and figure legend is from page 755 of Peter R. 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 18. Morphology of corystosperms. -A. Pachypteris papillosa stem with leaves, based on Harris (1983a, fig. 2): × 0.25 [transposed caption letters G, H, and I were corrected by J. M. Miller in 2008].

    -B. Pteroma thomasii synangium, abaxial view, redrawn from Harris (1964, fig. 66B); × 0.25.

    -C. P. thomasii, lateral view, based on Harris (1964, fig. 66A-G, I); × 2.

    -D. Dicroidium odontopteroides, redrawn from Thomas (1933, fig. 49a); × 0.75.

    -E. Umkomasia macleanii, redrawn from Thomas (1933, fig. 1, pl. 26, fig. 56); × 2.5.

    -F. Corystosperm ovule based on Thomas (1933, fig. 33c); × 4.

    -G. [I]. Rhexoxylon, transverse section of stem, based on Archangelsky and Brett (1961, fig. 2A); × 0.5.

    -H. [G]. Pollen of Pteruchus africanus, redrawn from Townrow (1962a, fig. 1A-D); × 2.5.

    -I. [H]. P. africanus, based on Townrow (1962a, fig. 1A-D); × 2.5."

    Most of the form genera of corystosperms are now known to be attached to massive trees (Dicroidium odontopteroides) that once formed a prevalent forest type on southern portions of Pangaea (Axsmith et al. 2000). The phylogenetic position of corystosperms as a group, is problematic (Klavins et al. 2002).

    Known gross morphological characters of the Corystospermales, and a list of phytophagous animal associates, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--shrubs and trees (M. E. White 1984)

    REPRODUCTIVE MODULES--cupules or carpel-like organs of Doylea tetrahedrasperma (Stockey and Rothwell 2009)

    The reproductive biology of corystosperms is not clearly understood, but some research progress has been made (Stockey and Rothwell 2009). Additional discoveries of permineralized sexual structures are needed to better understand these seed plants

    LEAVES--compound pinnate in general aspect (M. E. White 1984) or simple (Bomfleur et al. 2011)

    PHYTOPHAGOUS ASSOCIATE(S)--poorly understood

    PLANT IDENTIFICATION(S)--not applicable

    HOST SEED PLANT ORGAN(S) BEING EATEN--leaves (Dmitriev and Ponomarenko 2002)

    Frohlich in his update of the mostly male theory (MMT) of flower origins raises the interesting suggestion that early Mesozoic corystosperms might be flowering plant ancestors (Frohlich 2002). Despite an earlier assertion that the morphology of Pteroma supports MMT, there are problems in comparing the ovule morphology of flowering plants with corystosperms (J. A. Doyle 2008).

    Corystosperms represented by the Paleogene fossil Komlopteris cenozoicus, apparently survived the K-T asteroid impact, and co-occur with angiosperms, conifers, cycads, marine dinoflagellates, and ferns in a Tasmanian paleoflorule (McLoughlin et al. 2008). Some of the recent review papers on corystosperms include Axsmith et al. 2000, Klavins et al. (2002), Axsmith et al. (2007), and Stockey and Rothwell (2009).

    Publications on the paleobiology of corystosperms include a detailed survey of the group in the book by T. N. Taylor et al. (page 627, 2009) and papers by Bomfleur and Kerp (2010), Decombeix et al. (2010), and Bomfleur et al. (2011), among others.

    Pentoxylales. Taeniopteroid foliage, fragments of short-shoots, and reproductive structures were recovered from Jurassic sediments in the Rajmahal Hills of the Indian sub-continent and described as a new group of seed plants by Birbil Sahni in 1948. The fossil history and morphology of the group is reviewed by T. N. Taylor et al. (pages 768-773, 2009)

    Leaves attached to fragments of shoots of the whole plant Pentoxylon sahnii were first described as the form genus Nipaniophyllum.

    Taeniopterid leaves which were first described from several Australasian Jurassic fossil plant localities as Taeniopteris spatulata, are now known to be attached to whole plants referable to Pentoxylon. Detached ovulate axes were initially described as Carnoconites but now too, belong to Pentoxylon (Sahni 1948, Wesley 1963, among others).

    The image to the right is Figure 19 Peter R. 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 Peter Crane.

    "Figure 19. Morphology of Pentoxylon plants. -A. Carnoconites cranwelliae, ovulate heads, based on Harris (1962, text-fig. 2B, fig. 1): × 2.5 [transposed caption letters B and C were corrected by J. M. Miller in 2008].

    -B. [C]. Carnoconites, longitudinal section through ovule, based on Sahni (1948, fig. 21); × 10.

    -C. [B]. Nipaniophyllum raoi, redrawn from Sahni (1948, fig. 34 a,b); × 1.

    -D. Pentoxylon sahnii, transverse section of stem showing vascular strands, based on Sahni (1948, fig. 9); × 8.

    -E. Sahnia microsporangiate 'flower,' based on Vishnu-Mittre (1953, fig. 11) and Bose et al. (in press [1985]); × 2.5."

    Following in the footsteps of Sahni (1948), Vishnu-Mittre (1953) described pollen-bearing "flowers" of the Pentoxylales. Rao (1976, 1981) and others provide additional discussion of the relationships of the Pentoxylales with other gymnosperms.

    The anatomy, paleoecology, and taxonomy of pentoxylaleans indigenous to the Antarctic polar forest of Cretaceous times was reviewed by Howe and Cantrill (2001). In Mesozoic times these plants were probably shrub-like not unlike some of the bennettitaleans. Additional discussion of the biodiversity and paleobiogeography of this enigmatic seed plant group may be found in Wesley (1973) and T. N. Taylor et al. (2009), among other articles and books.

    Known gross morphological characters of the Pentoxylales, references, and future research needs are summarized below.

    WHOLE PLANT MORPHOLOGY--shrubs and trees? (T. N. Taylor et al. (2009)

    REPRODUCTIVE MODULES--ovulate clusters are described as Carnoconites. Howe and Cantrill (2001) provide a detailed discussion of the homologies of Carnoconites ovule-bearing spur shoots, which are almost certainly evolutionarily reduced megastrobili lacking laminar megasporophylls.

    Pollen-bearing cones and microsporophylls are absent and reduced to naked, stalked microsporangia arising from spur shoot apexes illustrated above and in Figure 19.25, page 771, T. N. Taylor et al. (2009)

    LEAVES--detached leaves have been described as Taeniopteris daintreei (see page 782, Figure 2, Howe and Cantrill 2001)

    PHYTOPHAGOUS ASSOCIATE(S)--unknown

    PLANT IDENTIFICATION(S)--not applicable

    HOST SEED PLANT ORGAN(S) BEING EATEN--not applicable

    There are few, if any anecdotal accounts of phytophagous animal associates of pentoxylaleans. Data are needed from study of existing museum specimens.


    Phylogenetic Considerations:

    This final chapter considers calibrating molecular phylogenies with fossils to improve accuracy and timing of seed plant divergences of angiosperms from the MRCA, use of concepts gleaned from biochemical studies of deeply conserved of cone and floral tool kits (Specht and Bartlett 2009), evo-devo of cones and flowers (Baum and Hileman 2006, Theißen and Melzer 2007, Hileman and Irish 2009, Melzer et al. 2010), and recent research on conifer cone abnormalities (Flores-Rentería et al. 2011, Rudall et al. 2011) to shed light on the origin of angiosperms and the flower.

    Student problems are posed at the end of this chapter, for purposes of character homology reassessment, data analysis, computation, and critique in the classroom and laboratory.

    The cartoon was drawn by Sul Ross State University geology student Mark Munday in 1981. The artwork by Mark, which is furnished David Rohr, Ph.D., and Mark's help at the delnortea beds is gratefully acknowledged.

    I assessed homologies of traditional seed plant characters, polarized these characters, and conducted two preliminary analyses from respective data matrices (Tables 4 and 5). Two separate phylogenies (one analysis includes two Devonian progymnosperm taxa) were computed using a standard maximum parsimony algorithm.

    An ontogenetic emphasis is considered in some aspects of my thinking, which is not unlike alternative ideas on character polarization in the absence of outgroups (Nelson 1978) and the concepts of biological and process-based homology (G. P. Wagner 1989, Laubichler 2000, Brigandt 2003) and heterochrony (Hufford 2002).

    I determined character polarities and rationale for assigning one-to-one correspondence along the lines proposed by Stevens (1984) and Zelditch and Fink (1996), but also considered a nested approach (H. E. Schneider et al. 2002).

    A prevailing view of many systematists, morphologists, and paleobotanists is that seed plants form a monophyletic group derived from early Devonian vascular land plant stock (Crane 1985, Rothwell and Serbet 1994, Hilton and Bateman 2006, J. A. Doyle 2006).

    I disagree with past ideas on a supposed monophyletic origin of seed plants. Based on models of fertile SAM organization derived from evo-devo research (Baum and Hileman 2006, Theißen and Melzer 2007, Melzer et al. 2010), pteridosperms might not constitute "the backbone of seed-plant phylogeny" (title, Hilton and Bateman 2006), but instead the supposed lineage might suffer from spinal bifida.

    Tool kits in homology. Students of paleobotany and seed plant phylogenetics should pay close attention to several elegant models of cone and floral organization, which are underpinned by basic biochemical studies of molecular tool kits and their demonstrably conserved suite of homeodomain proteins and cis-acting TFs of developing SAMs of bisexual cone axes (Theißen Saedler 2001, Becker and Theißen 2003, Theißen and Melzer 2007, Melzer et al. 2010).

    Models of deeply conserved molecular tool kits and transcriptional regulation suggest that several (at least two) lines of seed plant evolution might have existed 300 to 400 MYA, during the Devonian Period. Critically important pieces of the puzzle are missing because no extant model pteridosperm (e.g. Caytonia or Komlopteris) is available for study by plant biologists.

    Studies of the molecular evolution of KNOX/ARP homeodomain proteins (Beerling and Fleming 2007, Rosin and Kramer 2009), evolution of LFY genes following swarms of WGDs (Mouradov et al. 1998, Shindo et al. 2001, Vázquez-Lobo et al. 2007, Jiao et al. 2011), and molecular evolution of homeotic MIKC-Type MADS-box protein quartets (Theißen and Melzer 2007) are essential ingredients in understanding the evolution of cones, flowers, inflorescences, and flower-like organs.

    Modifications to the transcriptional machinery of seed plant SAMs could potentially lead to drastic changes in morphology of organs and reproductive modules, with profound implications toward traditional ideas of homology of seed plant organs. For example, carpels, cupules, fertiligers, integuments, microsporophylls, megasporophylls, ovules, and strobili are important in cladistic analyses of seed plants.

    This means that in disparate seed plant groups traditional ideas and supposed homologies of organs such as ovular integuments (origin by evo-devo splitting of tissues or by incorporation of foliar organs), and position of ovules on the megasporophyll whether adaxial or abaxial (Figures 13 and 14, J. A. Doyle 2006, Endress 2011), are called into question by studies of deeply conserved extant plant cis-acting TFs, regulatory genes, and tool kit proteins.

    Further, there is no convincing paleobotanical evidence for past elegant proposals on the evo-devo of the angiosperm outer ovular integument and carpels from cupules and axillary organs of Mesozoic Caytoniales to be found in the fast moving literature on molecular tool kits and ovular TFs (Kelley et al. 2009, Skinner and Gasser 2009, R. H. Brown et al. 2010, Tavares et al. 2010).

    Can angiosperm carpels share homology with the cupules of extinct seed plants if they were derived by completely different evo-devo programs of cis-acting transcriptional regulation?

    Canalization of sporophylls in relation to the SAM or lateral meristems might have evo-devo significance.

    A paper by C.-M. Feng et al. (2011) opens a window toward deciphering character homologies and morphological transitions by combining floral tool kit evo-devo with phylogenetics. Students of seed plant morphological phylogenetics should consider this approach.

    Top-down and bottom-up approaches. Molecular phylogenetics is also one of the most important tools in providing insight into the timing of the origin of angiosperms, evolution of the perianth, and diversification rates of the crown group of flowering plants (J. A. Doyle 2001, D. E. Soltis and P. S. Soltis 2003, Davies et al. 2004, Magallón and Sanderson 2005, Bateman et al. 2006, Sanderson and McMahon 2007, Hileman and Irish 2009, Magallón and Castillo 2009, Bell et al. 2010, Stephen A. Smith et al. 2010, Stephen A. Smith et al. 2011), despite a persistent long branch that separates extant flowering plants from gymnosperms (Sean W. Graham and Ihles 2009, Magallón 2010).

    Gene duplications may shed light on long branch attraction and other sources of errors during computation of molecular phylogenetic trees according to a critical analysis that contrasts "bottom-up" and "top-down" approaches (Bateman et al. 2006). Polyploidy including WGDs is one of driving forces behind diversification of the flowering plant clade (D. E. Soltis et al. 2007, Sanderson and McMahon 2007, Jaillon et al. 2009, D. E. Soltis et al. 2009, P. M. Soltis et al. 2009), and seed plant evolution as a whole (Jiao et al. 2011).

    A critique of phylogenetic approaches toward a better understanding of the origin of angiosperms and evo-devo of the ancestral flower by Bateman et al. (2006) suggests that too much reliance is placed on "empirical rigour" of large nucleotide and indel data matrices derived from very few extant plant species. Further, the review by Bateman, Hilton and Rudall states, "whereas morphology-based approaches increase the number of phylogenetically informative taxa (including fossils) at the expense of accessing only a restricted spectrum of phenotypic characters" (abstract, Bateman et al. 2006).

    Bateman et al. (2006) provide a detailed discussion of several questions posed in their review:

  • "What is a flower?
  • Which are the (other) benchmark studies in floral evolution?
  • Which are the benchmark studies in reconstructing seed-plant phylogeny?
  • Which kinds of phylogeny are of greatest value?
  • How significant are optimization and outgroups choice?
  • What is the best way to choose among the plethora of phylogenies?
  • What is the best way to assess the quality of a phylogeny?
  • Do some nodes in the land-plant phylogeny merit particular emphasis?
  • Why is it important that optimal taxon sampling dissects long branches?
  • What are the effects of culling taxa and/or characters?
  • What are the pros and cons of monophyly?
  • Which key characters best define the flower?
  • Why are palaeobotanists obsessed with extinct gymnosperms?
  • Are clades such as angiosperms best defined using taxa or characters?
  • Do some categories of character merit particular emphasis?
  • What is the preferred research programme for the next decade?"
  • Top-down and bottom-up approaches in unraveling the ancestry of seed plants and origin of the flower are reviewed by Specht and Bartlett (2009) and Rudall and Bateman (2010).

    Reviews on the origin of angiosperms and the flower by J. A. Doyle (1994, 2006, 2008), D. E. Soltis et al. (2008), Cibrián-Jaramillo and R. A. Martienssen (2009), Specht and Bartlett (2009), and Rudall and Bateman (2010), among others, outline 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) or Figure 1 on page 219 of Specht and Bartlett (2009) are places to begin discussion of top-down phylogenetic inference on the origin and relationships of stem- and crown-group flowering plants.

    Molecular phylogenetics. Key papers having to do with the big picture of molecular phylogenetics in lignophytes that were published during the last ten years include Barkman et al. (2000), Chaw et al. (2000), Savolainen et al. (2000), Wikström et al. (2001), Sanderson and J. A. Doyle (2001), Magallón and Sanderson (2002), Rydin et al. (2002), P. S. Soltis et al. (2002), Davies et al. (2004), Sanderson et al. (2004), Magallón and Sanderson (2005), Y. L. Qiu et al. (2005), Jansen et al. (2007), D. E. Soltis et al. (2008), Braukmann et al. (2009), Mathews (2009), H. E. Schneider et al. (2009), Tillich et al. (2009), de la Torre-Bárcena et al. (2009), Burleigh et al. (2011), and Jiao et al. (2011), among others.

    Older work is published by Martin et al. (1989), K. H. Wolfe et al. (1989), Bousquet et al. (1992), Hamby and Zimmer (1992), Chase et al. (1993), Martin et al. (1993), Savard et al. (1994), B. G. Baldwin et al. (1995), Barraclough et al. (1996), Goremykin et al. (1996), Sytsma and Baum (1996), Goremykin et al. (1997), D. E. Soltis et al. (1997), Chase and Albert (1998), J. A. Doyle (1998), Kuzoff et al. (1998), Nandi et al. (1998), P. S. Soltis and D. E. Soltis et al. (1998), Wolf et al. (1998), Mathews and Donoghue (1999), Parkinson et al. (1999), Samigullin et al. (1999), and P. S. Soltis et al. (1999), among others.

    Stephen A. Smith et al. (2010) report that the flowering plant crown group originated 217 MYA, which is the Norian Age of the late Triassic Period.

    Molecular phylogenetic analyses by Magallón (page 395, 2010) when calibrated with fossil data and compared with different relaxed-clock methods "... imply that the diversification that lead to living angiosperm species began sometime between the Upper Triassic and the early Permian."

    Phylogenetic studies of WUS homeodomain protein evolution (Nardmann et al. 2009), numerous molecular clock studies of phytochrome (Mathews and Donoghue 1999), and estimates gleaned from phylogenetic analyses of chloroplast and ribosome genes (Sanderson and J. A. Doyle 2001, Wikström et al. 2001, Magallón 2010, Stephen A. Smith et al. 2010), among others, suggest that seed plants split into the angiosperms and gymnosperms during the late Carboniferous or Permian periods of the Paleozoic Era about 300 MYA.

    Assertions and generalizations on a Mesozoic origin of flowering plants by certain paleobotanists are unsupported by molecular phylogenetic studies of the Class III HD-Zip gene family, which points to a gene duplication event leading to the PHABULOSA/PHAVOLUTA-related and CORONA/HB8-related clade about 300 MYA during the Carboniferous Period probably before to the angiosperm-gymnosperm split (Prigge and S. E. Clark 2006).

    Revised relaxed molecular clock estimates (Magallón 2010, Stephen A. Smith et al. 2010), and molecular phylogenetic studies of homeodomain proteins go along with revelations on the timing of WGDs in certain MIKC-Type MADS-box genes (S. Kim et al. 2004, Zahn et al. 20050, and timing of WGDs deduced from more rigorous genome models (Jiao et al. 2011). Specifically, the B-class MADS-box gene duplication in the AP3/PI genetic lineage that paved the way for the evo-devo of the first flower probably occurred roughly 230 to 290 MYA. (S. Kim et al. 2004).

    A possible paraphyletic Paleozoic origin of angiosperms contradicts proposals by Leebens-Mack et al. (2005) suggesting a monophyletic Mesozoic origin of a basal clade of flowering plants, which is based on estimates derived from cpDNA data.

    Douglas Soltis et al. (2011) published another broad molecular phylogenetic study of angiosperms, which is an ongoing subject of study by plant systematists all over the world.

    Morphological phylogenetics. Major milestone papers in morphological phylogenetics of lignophytes are authored by Crane (1985), J. A. Doyle and Donoghue (1986, 1987), J. A. Doyle et al. (1994, 1996, 2006), Nixon et al. (1994), Rothwell and Serbet (1994), Hickey and D. W. Taylor (1996), J. A. Doyle and Endress (2000), Hilton and Bateman (2006), and Rothwell et al. (2009), among others.

    Hörandl and Stuessy's recent review of paraphyly in plant systematics (2010) should be considered when defining the boundaries of evolutionary species using cytogenetic, genetic, genomic and phylogenetic tools. Simply put, not all higher level taxa in seed plant classification are monophyletic.

    Surprisingly, pteridosperms represented by the Paleogene fossil Komlopteris cenozoicus and Oligocene remains of Ptilophyllum muelleri survived the K-T extinction radiating with angiosperms and modern conifers in the forests of Tasmania (McLoughlin et al. 2008, McLoughlin et al. 2011).

    Discovery of a population of Cenozoic Corystospermales detracts from proposals such as MMT (Frohlich 2002). Existence of at least one post K-T bennettitalean population adds fuel to the idea that paraphyletic clades of anthophytes coexisted during the Cretaceous Period, up to- and after the Chichixulub bolide impact.

    Students of morphological phylogenetics now have ample grounds to question many published seed plant phylogenies. Albeit critical permineralizations of reproductive organs have yet to be described for several key orders and species of seed plants, rendering homology assessment and character scoring problematic at best.

    The graphic below represents a phylogenetic reconstruction of seed plants which was redrawn from J. A. Doyle (2008). Professor Doyle's tree represents the most parsimonious cladogram of his several phylogenetic reconstructions. I rotated the original drawing 45º to the right and left off other details including the number of steps and labels of higher orders of formal and informal classification. A detailed discussion of the analysis, character states, and the original data set may be found in the original paper (J. A. Doyle 2008).

    The preceding graphic is redrawn from Fig. 6 on page 827 of J. A. Doyle (2008), Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower, International Journal of Plant Sciences 169(7): 816-843.

    Some of the seed fern groups are colored indigo brown on the dendrogram shown above. Corystosperms and glossopterids appear in blue typescript. Bennettitaleans are denoted by the reddish-brown type-face. Pentoxylales are colored pink on the chart. Gnetophytes, once regarded as a sister group to flowering plants (J. A. Doyle and Donoghue 1986, 1987; Donoghue and J. A. Doyle 2000) are displayed as purple letters. Cycadales and Caytonia are shown on the graphic in green letters. Common groups of conifers and the ginkgos appear in brown type. Finally, some of the critical fossil groups of flowering plants and extant angiosperms are depicted in red type.

    Important reviews of seed plant phylogeny including angiosperms by Crane (1985), J. A. Doyle and Donoghue (1986), J. A. Doyle and Donoghue (1987), Loconte and Stevenson (1990), J. A. Doyle and Donoghue (1993), Nixon et al. (1994), Rothwell and Serbet (1994), J. A. Doyle (1998), C. N. Miller, Jr. (1999), J. A. Doyle (2001), J. A. Doyle (2006), Hilton and Bateman (2006), D. W. Taylor et al. (2006), Erbar (2007), J. A. Doyle (2008), Chase and Reveal (2009), J. A. Doyle (2009), Mathews (2009), and Rothwell et al. (2009), overlook several groups of possibly important Paleozoic stem group gymnosperms.

    Two overlooked Permo-Carboniferous seed plant groups: Vojnovskyales (Mamay 1976) and gigantopterids (page 162, G. Sun et al. 2001) have been discussed as possible angiosperm ancestors. Gigantopteroids discussed by Mamay et al. (1984), Mamay et al., (1988), and by Ricardi et al. (1999) will require serious consideration as potential ancestors of the flowering plants (see next section).

    Vojnovskyales constitute a small order of hermaphroditic gymnosperms with monocot-like foliage known from rocks of Carboniferous Period (Mamay 1976, Rothwell et al. 1996, Naugolnykh 2001). Students should note that these seed plants with their bisexual cone axes existed during the interval in deep time when molecular phylogenetic data suggest that the angiosperms diverged from the MRCA (Bowe et al. 2000).

    Albeit, Mamay's review (page 295, 1976) was uncomplimentary however, the taxon in question (Vojnovskya), the original publication by Professor Maekawa (in Japanese), and sister genera of Vojnovskyales should be evaluated and incorporated into phylogenetic analyses and discussions of seed plant evolution. Rothwell et al. (1996) is one of the only papers that evaluates Vojnovskyales from a phylogenetic research perspective.

    Oleanane containing Permian seed plants (Moldowan and Jacobson 2002) known as gigantopterids, are missing from almost all phylogenetic trees published in the literature, with the exception of D. W. Taylor et al. (2006). This is understandable because fossilized reproductive material (X.-G. Li and Z.-Q. Yao 1983) is controversial, fragmentary, and inadequately described as morphotype genera.

    Original papers by Asama (1960, 1982) and H. D. Zhang (cited in G. Sun et al. 2001) detailing an origin of flowering plants from gigantopterids will require reanalysis and discussion within the contexts of coevolution and heterochrony. Gigantopteroids, specifically Delnortea abbottiae and Evolsonia texana should be evaluated independently as they might be unrelated to gigantopterids and Peltaspermales.

    Hypothetical protoflowers of gigantopteroids. In the first essay on the Origin of Angiosperms I discussed a recent paper by Rothwell et al. (2009), revisited the main hypotheses on the origin of flowering plants and the flower, and proposed a novel hypothesis based on molecular coevolution of insect and seed plant developmental tool kits and CRMs.

    Did some seed plant populations "start blooming" during the Permian or Carboniferous Period? Possibly.

    I also stated that a few elements of the anthophyte hypothesis (Donoghue and J. A. Doyle 1986) and classic research by Arber and Parkin (1907), Edgar Anderson (1934), Ehrlich and Raven (1964), Raven and Kyhos (1965), Takhtajan (1969, 1976), and Raven (1977), dovetail with- and potentially support a coevolutionary hypothesis on the origin of flowering plants.

    Piecing together fossil evidence mined from Upper Paleozoic rocks. Ostensibly one of the more important Permo-carboniferous puzzles to piece-together is the whole plant morphology of Delnortea and Evolsonia gigantopteroids to include detached, retuse Taeniopteris multinervis and "Phasmatocycas sp." leaf fossils, which are almost always preserved in the same rock layers together with abscised gigantopteroid foliage and shed cordaicarp ovules (DiMichele et al. 2000). Were all these pieces part of the same Delnortea or Evolsonia mother plant?

    Rothwell et al. assert (page 317, 2009) that missing links and "transformational series" in the fossil record in support of the anthophyte hypothesis have yet to be discovered. These workers overlook potentially important clues from detailed anatomical studies of pieces of detached fertile Paleozoic leaves once thought to be related to cycads (Axsmith et al. 2003), or compare evolutionarily precocious and innovative leaf anatomy (Mamay et al. 1988), and venation density patterns (Boyce et al. 2009) of oleanane-containing Permian gigantopterids (D. W. Taylor et al. 2006) to Bennettitales, Gnetales, and eudicot flowering plants.

    While the whole plant morphology of Permo-Carboniferous gigantopteroid and Phasmatocycas gymnosperms remains a mystery detached pieces of ovule-bearing Phasmatocycas bridwellii megasporophylls, undescribed microsporangia-bearing leaves (preceding section), and gigantopteroid-like petaloid organs (discussed herein), might be fragments of a protoflower with a well-defined perianth and elongated or conical Magnolia-like receptacle.

    The diagram below is a reconstructed longitudinal section of the short shoot and floral organ of a hypothetical gigantopteroid seed plant. A 25-centimeter broad bracteopetaloid perianth consisting of retuse Lonesomia mexicana-like taeniopteroid tepals is diagrammed. The hermaphroditic spur shoot attached to a small tree, pachycaulous shrub, or vine-like mother plant might have been subtended by clasping gigantopteroid leaves clothing a long shoot or vegetative branch.

    Spirally-arranged tepals might have been attached to the base of a shortened hermaphroditic cone axis illustrated above, which was not unlike the fertile spur shoot of Ginkgoales. Just inside a spiral of several tepals, a third ring might have consisted of several spirally arranged UV-absorbing and/or colored andropetals, which are enclosing an inner ring of microsporangium-bearing leaves (microsporophylls). The leaf-like microsporophylls might have clasped an innermost ring of Phasmatocycas bridwellii-like ovule-bearing megasporophylls.

    The hypothetical Ginkgo-like spur shoot, which is illustrated in the preceding diagram, might have been subtended by an Evolsonia-type gigantopteroid megaphyll.

    Are unambiguous fossils of whole bisexual gigantopteroid protoflowers known from Paleozoic rocks? No.

    There are four examples of detached pieces and whole plant fragments known from Carboniferous and Permian sediments which have been described and illustrated by Axsmith et al. (page 1586, Figures 1-5, 2003), Mei et al. (page 101, Plate 2, 1992), R. Weber (page 232, Plate 3, 1997), and T. N. Taylor et al. (page 713, Figure 17.23, 2009). A color image of a Phasmatocycas bridwellii distal branch (I interpret this fossil as an incomplete proanthostrobilus) is provided by T. N. Taylor et al. (page 710, Figure 17.15, 2009).

    A fifth example was offered by X. Li and Yao (page 26 and Plate 4, 1983), but these might be evolutionarily unrelated to Delnortea, Eophyllogonium, Evolsonia, and Lonesomia.

    Were the gigantopterids described by X. Li and Yao in 1983 actually peltaspermaleans? Possibly, according to T. N. Taylor et al. (2009).

    The Paleozoic fossil Sobernheimia jonkeri (Kerp 1983; page 713, Figure 17.23, T. N. Taylor et al. 2009) might also be detached megasporophylls of a massive bisexual gigantopteroid protoflower with the microsporophylls and perianth also shed and therefore, evading a complete diagnosis of the whole fertile SAM.

    Further, attachment points of some Paleozoic taeniopterid laminae are remarkably similar to tepal bases of ANITA grade basal angiosperms (page 847, Figure 2, Endress 2008). Unfortunately, it is not clear from Reinhard Weber's 1997 paper where taeniopteroid laminae were attached to the whole gigantopteroid plant.

    Paleozoic rock layers that yield detached gigantopteroid leaves with clasping leaf bases are often accompanied by taeniopterid leaves possessing wedge-shaped bases. The possibility should be entertained that both kinds of leaves came from the same deciduous plant. Taphonomic data are needed in most cases when unearthing and cataloging leaf-bearing Permian rock beds. Paleontologists should also be on the lookout for stem fragments with preserved leaf bases in gigantopterid-bearing sedimentary layers. Oleanane TSB data are needed in most cases.

    Detailed paleobotanical studies of the anatomy and morphology of obscure, poorly studied Paleozoic and Mesozoic gymnosperms are needed to fill in the considerable gaps in existing data sets before phylogenetic analyses can be calibrated with minimum fossil ages (Gandolfo et al. 2008). Yet, one recent paper proclaims:

    "The oracle whether the angiosperms arose via rapid accumulation of the synapomorphies that characterize flowering plants (the carpel, double fertilization, flower) or through gradual accumulation of these traits over longer time (the 'transitional-combinational theory', Stuessy 2004) remains unanswered although results from 'evo-devo' research support the possibility of a more or less sudden flower origin. The coincidence between the origin and diversification of the class E genes, the duplication event in the class B genes, the decoupling of C and D function and the origin of angiosperms (Fig. 9) suggests that these genes are involved in the processes that made possible the morphological invention of the flower."

    The preceding passage is quoted from page 127 of Erbar (2007), Current opinions in flower development and the evo-devo approach in plant phylogeny, Plant Systematics and Evolution 269: 107-132.

    Possessing a perianth of taeniopteroid tepals and andropetals attached to the Gingko-like spur (short) shoot of a massive protoflower subtended by a vegetative gigantopteroid leaf (the whole plant had dimorphic leaves, thus exhibiting heteroblasty), delnorteas and evolsonias were completely new and different kinds of Upper Paleozoic gymnosperms. Gigantopteroids were probably indigenous to coastal, upland or marginal environments, away from swamps and seeps of the region, which were dominated by giant lycophytes or squat Pleuromeia plants, horsetails (sphenopsids), and medullosan pteridosperms.

    Conclusions reached by Bharti Sharma et al. (2011) on evo-devo studies of paralogs of AP3 in Aquilegia suggest that:

    "... the AqAP3-3 lineage underwent progressive subfunctionalization within the order Ranunculales, ultimately yielding a specific role in petal identity that has probably been conserved, in stark contrast with the multiple independent origins predicted by botanical theories."

    The above statement is from the abstract of Bharti Sharma, C. Guo, H. Kong, and E. M. Kramer, (2011), Petal-specific subfunctionalization of an AP3 paralog in the Ranunculales and its implications for petal evolution. New Phytologist 191(3): 870-883.

    Based on supposed deep conservation in AP3 and the TFs they encode, were some of the traits expressed in taeniopteroid tepals of gigantopteroid protoflowers possessing retuse apices and Clusia-like venation patterns representative of early petals?

    We should not forget that classical paleobotanists pieced together whole Lepidodendron (Lepidodendrales, Lycophyta) and Psaronius (medullosan pteridosperm) trees from fossilized detached parts originally described as morphotype genera.

    "Perhaps the greatest biofantasy of whole-plant reconstruction is the misconception that organ attachment is the only way to ascertain organ association in an acceptable manner."

    This statement is quoted from page 147 of W. A. DiMichele and R. A. Gastaldo (2008), Plant paleoecology in deep time. Annals of the Missouri Botanical Garden 95: 144-198.

    Therefore, it is possible that some detached, sterile, retuse, heteroblastic taeniopteroid "petals," gigantopteroid megaphylls, and Phasmatocycas-like megasporophylls catalogued and distilled in T. N. Taylor et al. (2009), might be fragments of the same seed plant species or represent whole new gymnosperm genera and taxonomic orders.

    Paleozoic protoflowers and their biological implications. The hypothetical protoflower of a gigantopteroid is potentially equivalent to J. A. Doyle's proanthostrobilus concept (2006), and the ancestral angiosperm flower with all attendant biological and evolutionary implications expressed in the Strobilus Theory of the Angiosperm Fructification (page 37 and Figure 1 on page 44, Arber and Parkin 1907); and by Crane (1985), J. A. Doyle and Donoghue (1986), J. A. Doyle (2008), Endress (2008), Endress and J. A. Doyle (2009), Hileman and Irish (2009), and Sage et al. (2009).

    When supported by paleobotanical evidence how would the existence of 300 million year old protoflowers with a differentiated perianth of tepals (andropetals or bracteopetals) dovetail with a "Mosaic Theory for the Evolution of the Dimorphic Perianth" (page 3571, Warner et al. 2009)?

    While discussing fossilized "distinct clusters" of fertile and sterile taeniopterid leaves on page 1591 Axsmith et al. (page 1586, Figure 1, 2003) introduce the descriptor "flushes" to the reader.

    Could the term "flush" be replaced with the horticultural term "blossom" when describing an anthocyanic hypothetical bisexual proanthostrobilus of a Paleozoic seed plant?

    Some of these hypothetical gymnosperms with protoflowers might possibly represent fertile natural intergeneric hybrids arising in long extinct populations of sympatric gigantopteroids and Vojnovskyales.

    When whole seed plants are reconstructed from fossilized detached parts, the resulting species and character analyses may be critical in unraveling potential reticulations in paraphyletic lines of gymnosperms existing at the time of the divergence of angiosperms from the MRCA bracketed by molecular clock studies (Magállon 2010), but also based on the timing of swarms of seed plant WGDs modeled by Jiao et al. (2011) occurring prior to the EPE but after the DeCARB.

    Fossil calibrations e.g. using the gigantopteroids Delnortea abbottiae, Evolsonia texana, and certain Vojnovskyales are clearly needed to narrow-down the timing of the MRCA of flowering plants, and other "great" late Paleozoic gymnosperm divergences of the Coniferales, Cycadales, Ginkgoales, and Gnetales (see subsequent chapters).

    While discussing salient findings of key papers published during the last decade of the 20th Century, the anthophyte hypothesis, and refutation of the idea that Gnetales are related to angiosperms, Friis et al. (2005) assert:

    "As a result, the relationships of angiosperms remain uncertain and the prospects for understanding the origin of characteristic angiosperm features, such as the carpel and stamen, are as remote as ever."

    I disagree with this opinion. Why?

    A possible answer rests with a large body of convincing evidence from biochemical and genetic studies of molecular tool kits, which is discussed in the first essay and restated in the next subsection.

    Evidence from deeply conserved tool kits. Elegant models of cone and floral organization (Baum and Hileman 2006, Theißen Saedler 2001, Becker and Theißen 2003, Theißen and Melzer 2007) supported by in-depth knowledge of tool kit cone and floral CRMs (Moyroud et al. 2009, Melzer et al. 2010, Moyroud et al. 2010), predict the construct of a Permo-Carboniferous protoflower.

    Cone and floral tool kits are too conserved, possibly developing in several late Paleozoic gymnosperm populations, to somehow accommodate bizarre morphologies seen in Mesozoic Caytoniales within a logical chronocline leading to the Amborellanae, Austrobaileyanae, Nymphaeanae, and Magnolianae.

    Further, our knowledge of carpel, floral, and ovular TFs in extant angiosperm model organisms does not preclude derivation of evo-devo models that explain curling, inrolling, and fusion in 300 million year old ovule-bearing gigantopteroid Phasmatocycas bridwellii leaves to form carpels, ovaries, and pistils.

    One hundred and sixty million years of neotenic evolution to include condensation of hypothetical gigantopteroid protoflowers could be the most simple evo-devo process to explain the origin of reproductive organs in Mesozoic crown group angiosperms and extant basal Amborellanae, Austrobaileyanae, Nymphaeanae, and Magnolianae.

    "... Equally puzzling is that despite intense interest in the origins of seed plants and angiosperms throughout the entire last century, few have looked at the problems from a life cycle evo-devo perspective, with perhaps one exception (Takhtajan 1976), who alluded to neoteny as one of the possible mechanisms contributing to the origin of angiosperms."

    The above quotation is from page 296 of Y.-L. Qiu (2008), Phylogeny and evolution of charophytic algae and land plants. Journal of Systematics and Evolution 46(3): 287-306.

    Based on molecular phylogenetic studies of MYB TFs in seed plants and arthropod olfactory and nuclear receptors and vision-related proteins indicating a conserved evolutionary history, it would not be unreasonable to propose that the hypothetical protoflower illustrated above might have attracted (or repelled) large phytophagous insects including paleodictyopterans. Geochemical studies screening for oleonone triterpanes among detached fragments of bisexual cone axes in the same bedding plane might be worth conducting in the future.

    Dating angiosperm divergences from the most recent common ancestor (MRCA). Precise dating of the putative "Great Late Paleozoic Gymnosperm Divergences" of conifers, cycads, ginkgophytes, and gnetophytes, and splits of angiosperms from the MRCA, is problematic but absolutely necessary.

    What is interval in geologic time when angiosperms diverged from the MRCA as determined from molecular substitution data, relaxed-molecular clock estimates, and timing of WGDs?

    Should plant biologists who compute tool kit phylogenies routinely calibrate molecular divergence times with paleobotanical evidence i.e. fossils?

    Ancient WGDs are implicated in both the common ancestor of eudicots and monocots, and in the MRCA of seed plants, and the flowering plants, roughly coinciding with the DeCARB and TrCCE. Further, an exhaustive genomic study of the cultivated grape overwhelmingly supports the existence of paleohexaploidy (Jaillon et al. 2007), which is equivalent to the "γ triplication" cited by Jiao et al. (2011).

    Stephen A. Smith et al. (2010) report that the flowering plant crown group originated 217 MYA, which is the Norian Age of the late Triassic Period.

    Molecular phylogenetic analyses by Magallón (page 395, 2010) when calibrated with fossil data and compared with different relaxed-clock methods "... imply that the diversification that lead to living angiosperm species began sometime between the Upper Triassic and the early Permian."

    Based on morphology alone, the explosion of diversity of phytophagous coleopterans and dipterans following the EPE predates the oldest known flowering plants by more than 100 million years. Yet, certain paleobotanists and plant ecologists incorrectly assert that angiosperms originated suddenly during the Cretaceous Period.

    This view contrasts with rbcL molecular clock estimates by Savard et al. (page 5166, 1994) who estimate the interval in geologic time when "extant seed plants shared their last common ancestor," between 275 and 295 MYA during the early Permian or late Carboniferous periods.

    Assertions and generalizations on a Mesozoic origin of flowering plants by certain paleobotanists are unsupported by molecular phylogenetic studies of the Class III HD-Zip gene family, which points to a gene duplication event leading to the PHA/PHAV-related and CORONA/HB8-related clade about 300 MYA during the Carboniferous Period possibly probably before roughly estimated timing of the angiosperm-gymnosperm split (Prigge and S. E. Clark 2006).

    Revised relaxed molecular clock estimates (Magallón 2010, Stephen A. Smith et al. 2010) and molecular phylogenetic studies of homeodomain proteins go along with revelations on the timing of WGDs in certain MIKC-Type MADS-box genes (S. Kim et al. 2004, Zahn et al. 2005). Specifically, the B-class MADS-box gene duplication in the AP3/PI genetic lineage that paved the way for the evo-devo of the first flower probably occurred 230 to 290 MYA (S. Kim et al. 2004).

    Charles Bell et al. (2005), in an early phylogenetic analysis, age the crown group of angiosperms from 106.1 to 229.4 MYA. Another estimate of the age of angiosperms determined by penalized-likelihood methodology is 251.77 MYA (H. E. Schneider et al. 2004), based upon Bayesian relaxed-clock methods (J. L. Thorne and Kishino 2002).

    Five years later Bell and coworkers refined their approach while employing more than 560 taxa and 35 calibration points (Bell et al. 2010).

    Calibrating points of divergence in geologic time using molecular substitution data is tricky (Graur and Martin 2004) and the subject of continuing debate. When calibrating divergence times in molecular phylogenies, students ought to pay more attention to simple methodology devised by paleontologists (Marshall 2008) or cutting edge, computer simulation studies that clearly demonstrate the critical importance of fossils (Quental and Marshall 2009).

    A couple of invertebrate paleontologists and computational theorists have recently published papers which address these problems and the possibility that rates of divergence vary in lineages over geologic time (Quental and Marshall 2010). Molecular plant systematists are also adopting these methodologies (Stephen A. Smith et al. 2011).

    "Despite the singular ecological significance and species diversity of angiosperms, they are not in a genealogical sense one of the major branches of land plants and did not originate with other major land plant clades (e.g. lycopsids, ferns, conifers, cycads, ginkgos) during the middle or late Paleozoic."

    The preceding quotation is from page 380 of S. L. Wing and L. D. Boucher (1998), Ecological aspects of the Cretaceous flowering plant radiation. Annual Review of Earth and Planetary Sciences 26: 379-421.

    Despite wide disagreement on the timing of the angiosperm-gymnosperm split, there is growing consensus among some molecular systematists and paleobotanists on the potential existence of a 160 million year old ghost lineage of flowering plants.

    In conclusion, molecular dating of the angiosperm divergence from the MRCA remains an important piece of the puzzle, which could allow paleobotanists to better focus their quest for the ancestor of angiosperms (or its detached pieces) in late Paleozoic rocks. "The Great Late Paleozoic Gymnosperm Divergences" coined here, have yet to be properly calibrated sensu Marshall (2008) with 300 million year old gigantopteroid and vojnovskyalean protoflower fossils.

    Evo-devo of progymnosperm and seed plant SAMs: Paleozoic splits. I concluded in the first essay on the origin of angiosperms that cladogenesis of flowering plants may be traced back in geologic time to the EPE and to surviving remnants of already divergent Permian seed plant lineages.

    Clues gleaned from biochemical studies of vegetative growth and SAM organization in extant model lignophytes and monilophytes, when combined with insight gained from molecular phylogenetic analyses of Class III HD-Zip genes and KNOX homeodomain proteins suggest that at least two (possibly three or more) evo-devo programs potentially existed in early diverging Devonian lycopsid, progymnosperm, and seed plant populations.

    If this hypothesis is correct then traditional ideas on the homology of leaf and sporophyll characters, which are gene expression products of TFs downstream of the SAM patterning developmental tool kit, should be reconsidered.

    Joel Cracraft (page 349, 2005) brings several "issues" to the table regarding evo-devo and homology, which have a bearing on supposed homologies of seed plant reproductive structures and the present analysis (the comment in brackets [] is mine):

  • "If evo-devo is also about evolution [it certainly is, see reviews by Raff 2000, G. B. Müller 2007], how is the evolution of development among taxa to be studied?
  • What are the developmental characters (entities) being compared?
  • Does it mean that the observations ('characters') of evo-devo are merely to be mapped on a tree of choice?
  • Or do the comparative observations themselves have a contribution to make about relationships, alternative hypotheses of which affect interpretations of change?
  • In short, can evo-devo advance as an evolutionary discipline using biological homology, process homology, or other similar concepts?"
  • Several important reviews discuss from morphological, paleobotanical, and phylogenetic research perspectives, the evo-devo of innovative morphologies in divergent Devonian vascular plant lineages (Boyce and Knoll 2002, H. E. Schneider et al. 2002, Friedman et al. 2004, J. A. Doyle 2006, Hilton and Bateman 2006, Stein and Boyer 2006, Beerling and Fleming 2007, David-Schwartz and Sinha 2007, Sanders et al. 2007). All the preceding papers were overlooked in a general review of the evolution of developmental mechanisms in plants by Langdale (2008).

    I agree with some of the philosophical arguments published by H. E. Schneider et al. (page 331-332, 2002), which were employed in their analyses of "new sources of data to answer long-standing questions about plant evolution," namely "integration of phylogenetic reconstruction, morphological studies, and developmental genetic data" through phylogenetic inference based on "a series of nested studies" (the phrase in brackets [] is mine):

  • (1) adoption of nucleotide sequence data gleaned from biochemical studies of coding and/or non-coding regions,
  • (2) making use of anatomical, biochemical, cytological, and morphological data sets to infer character evolution,
  • (3) comparison of these sets of data with gene trees of key developmental genes and evo-devo programs, and
  • (4) casting the results in light of a fundamental trend observed in vascular plant evolution that body plans simplify [by neoteny] over the course of deep time.
  • The state of evo-devo biology has progressed much since H. E. Schneider and colleagues published their book chapter in 2002. Some aspects of the traditional Hennigian concept of homology have been challenged by insight gained from studies of transcriptional regulation by homeotic CRMs (Abouheif 1997, Abouheif et al. 1997, Janies and DeSalle 1999, Wray 1999, Brigandt 2003, Theißen 2005, Rosin and Kramer 2009, Theißen 2009).

    Peter Endress (2003) suggests that combined developmental and paleobotanical studies might shed more light on solving perplexities of perianth evolution in extant basal angiosperms of the crown group. His ideas are further developed in a second review (Endress 2011).

    Taking into account critical reevaluation and discussion of the homology concept when dealing with morphological characters determined by CRMs, it may be necessary to modify and/or add to the "nested" approach used by H. E. Schneider et al. (page 331-332, 2002), restated in bulleted form, above. That is, the third and fourth bulleted lines of evidence might be considered before conducting the character analyses (item 2).

    "It is first necessary to have phylogenetic evidence that observed differences in gene expression are meaningful in terms of morphological evolution."

    This quote was transcribed from page 163 of L. Reiser, P. Sánchez-Baracaldo, and S. Hake (2000), Knots in the family tree: evolutionary relationships and functions of KNOX homeobox genes. Plant Molecular Biology 42(1): 151-166.

    Molecular phylogenetic studies of WUS-WOX homeotic TFs (Nardmann et al. 2009), numerous molecular clock studies of phytochrome (Mathews and Donoghue 1999), chloroplast, and ribosome genes (reviewed by Sanderson and J. A. Doyle 2001, Wikström et al. 2001), and revelations on the timing of WGDs in certain MIKC-Type MADS-box genes (S. Kim et al. 2004, Zahn et al. 2005) point to a late Carboniferous or Permian divergence of seed plants into the angiosperms and gymnosperms.

    Vásquez-Lobo et al. (2007), in an elegant study of FLO/LFY orthologs in Picea (Coniferales), Podocarpus (Podocarpales), and Taxus (Taxales), while employing ultrasensitive radioactive probes and histochemical methods, clearly demonstrate in situ expression of FLO/LFY gene transcripts in all the organs of female fertile SAMs. Shindo et al. (2001) suggest:

    "Thus, it is likely that the induction of MADS-box genes by FLO/LFY homologues was established after ferns diverged from the seed plant lineage but before extant gymnosperms and angiosperms diverged."

    The preceding passage is quoted from page 1205 of Shindo et al. (2001), Characterization of FLORICAULA/LEAFY homologue of Gnetum parvifolium and its implications for the evolution of reproductive organs in seed plants. International Journal of Plant Sciences 162(6): 1199-1209.

    Certain homeodomain proteins (e.g. KNOTTED1), FLO/LFY proteins, phytohormones, and other small-sized (<60 kilodalton) TFs and their mRNAs move from cell to cell via plasmodesmata in the SAMs of some of the model eudicot angiosperms studied (Jackson 2002, J.-Y. Kim et al. 2003, Jackson 2005). Experimental data are needed to verify trafficking of homeodomain TFs and FLO/LFY proteins in fertile SAMs of extant flowering plants and gymnosperms.

    A paper by Pham and Sinha (2003) on the evo-devo of a non-model gnetophyte does not address potential significance of KNOX homeodomain protein movements from the SAM to leaf primordia, thence to regions of indeterminate growth, when discussing ontogeny of accessory scaly bodies and reproductive organs in Welwitschia mirabilis.

    The physiology of SAM macromolecular trafficking involving phytohormones when extrapolated to seed plants in deep time is an important component of two prevailing models of cone organization and floral origins (Baum and Hileman 2006, Theißen and Melzer 2007).

    Two or more traffic patterns of homeodomain protein movement and phytohormone flow might have emerged in meristems of aerial shoots of extinct progymnosperms and seed plants, but paleontologic evidence from studies of permineralized cells and tissues is lacking.

    Clues on the possible existence of polar auxin flow in woody stems have been uncovered in comparative anatomical studies of a 375 million year old fossilized progymnosperm known as Archaeopteris and modern conifers (Rothwell and Lev-Yadun 2005). The fossil record reveals that auxin regulation of secondary growth was a conserved physiologic process (Rothwell et al. 2008).

    Did KNOX proteins, among others, move from cell-to-cell in the SAMs and axillary SAMs of extinct Paleozoic vascular plants?

    Baum and Hileman (page 16, 2006) propose that since the gibberellin signaling pathway positively regulates LFY gene expression (and LFY integrates fertile meristem ontogenetic change from vegetative to reproductive), the bisexual cone axis in "... the common ancestor of angiosperms and gymnosperms [MRCA] would have gradually accumulated higher and higher levels of LFY protein during development." The acronym in brackets [] is mine.

    When considering the evo-devo of SAM developmental programs in deep time, conceptual models that incorporate movable homeodomain proteins and CREs, have potentially profound implications toward evolution of leaves, sporophylls, and lycopsid, progymnosperm, and seed plant reproductive axes.

    Seed plant morphologies such as the arrangement of sporophylls on the mother plant and position of ovule attachment (terminal, abaxial, adaxial, or marginal) to stems and/or leaves potentially reflect diverse mechanisms of homeodomain protein trafficking in SAMs (at the organismal level), and evolution of modular units and cis-acting TFs in paleopopulations.

    Many of the supposed homologies of leaves, sporophylls, and ectopic structures including reproductive axes and ovular integuments could be incorrect based on the possibility that a fundamental dichotomy in SAM evo-devo emerged in Devonian vascular plant stock. Lateral branches of the Devonian progymnosperm, Archaeopteris (Archaeopteridales) may arise from tissue fields resembling leaf primordia, and not axillary buds (page 481, T. N. Taylor et al. 2009).

    Hickey and D. W. Taylor (1994) regard fertile axes of some seed plants as fertile trusses derived from telombs. There is no evo-devo evidence from the study of SAM maintenance and patterning genes and TFs supporting of Zimmermann's Telomb Theory. More research is needed.

    Character analysis and homology assessment. A review of homoplasy by Wake et al. (2011) is available. Evolution of ontogenetic sequences and their homologies is reviewed in a book edited by Zelditch (2001).

    Rothwell et al. (2009) state that no known seed plant fossil transformational series supports past proposals on derivation of the angiosperm carpel and ovule integuments from Caytonia-like cupules, or the MMT. Professor Rothwell's quite correct insight from fossil record is incongruous with the idea floated by Specht and Bartlett (page 220, 2009) that extant gymnosperms "are sufficiently divergent from angiosperms to prevent reliable reconstruction of flower origins."

    Are studies by Flores-Rentería et al. (2011) and Rudall et al. (2011) of recurrent flower-like abnormalities in conifer cones consistent with these ideas?

    Inclusion of pteridosperms such as Caytonia or corystosperms (and their glossopterid ancestors) in a morphologically based phylogenetic analysis of angiosperms might be fundamentally flawed on evo-devo grounds (bulleted list and question posed, above).

    How does this opinion fit with studies of ovule determinants by Gasser, Skinner, and co-workers, and recent reviews of xylem heterochrony (Carlquist 2009), seed evolution (Linkies et al. 2010), and the evo-devo of secondary xylem of lignophytes (Rachel Spicer and Groover 2010), among others?

    Some of the aforementioned problems in seed plant homology and character analyses are explored from an experimental cladistic perspective to simplify data analysis and to ameliorate certain vexing problems in seed plant morphological phylogenetics (J. A. Doyle and Endress 2009).

    Homologies of the carpel and stamen. Reviews by D. W. Taylor and Kirchner (1996), Friedman et al. (2004), J. A. Doyle (2006), Scutt et al. (2006), Endress and J. A. Doyle (2009), Specht and Bartlett (2009), and Vialette-Guiraud and Scutt (2009) outline the great body of literature which has been devoted to evolutionary and experimental cladistic studies of carpel homologies.

    A solitary carpel of the "living fossil" magnoliid tree, Degeneria vitiensis (Degeneriaceae, Magnoliales), is depicted in the left-hand scanning electron micrograph, ×15. The right-hand image is a scanning electron micrograph of a Degeneria microsporophyll, ×5.

    The Degeneria reproductive organs were field-fixed in 1986 and 1987 from dissected flowers collected in the canopies of tagged and vouchered trees growing in stands on the slopes of Mount Naitaradamu on Viti Levu Island, and from forested flanks of Mount Delaikoro, Vanua Levu Island, Fiji.

    The scanning electron micrographs were prepared by Al Soeldner, Director, Oregon State University Electron Microscopy Laboratory. I thank the National Geographic Society for providing research funding for this study.

    David Winship Taylor and Kirchner (page 119, 1996) provide a detailed discussion of the "phyllosporous origin" and "stachyosporous origin" hypotheses of carpel homologies.

    The homology assessment of the angiosperm carpel, perianth, and flower by D. W. Taylor and Kirchner (Figure 6.3 page 124, 1996) would be confounded by the inclusion of a hypothetical Paleozoic gigantopteroid protoflower.

    Phyllosporous origin hypotheses. The phyllosporous origin hypotheses is also coined the "megasporophyll-homology hypothesis" (page 119, D. W. Taylor and Kirchner 1996). Serge Mamay (Figure 7, page 33, 1976) was a 20th Century paleobotanist who proposed a conduplicately-folded megasporophyll hypothesis for a Paleozoic origin of Cycadales, but this fact apparently went unnoticed by D. W. Taylor and Kirchner twenty years later (1996).

    David Winship Taylor and Kirchner's megasporophyll-homology hypothesis is based on morphological studies of primitive magnoliids by I. W. Bailey and Swamy (1951). The carpel of Degeneria vitiensis (Degeneriaceae, Magnoliidae) shown in the image on the left side of this page, was thought to be a conduplicately folded (inrolled) megasporophyll (I. W. Bailey and A. C. Smith 1942).

    Evolutionary developmental research on carpel, floral, and ovular transcriptional regulators in extant angiosperm model organisms (Scutt et al. 2006) do not preclude derivation of models of cone- and floral organization that explain curling, inrolling, and fusion in 300 million-year-old ovule-bearing gigantopteroid Phasmatocycas bridwellii megasporophylls to form carpels, ovaries, and pistils.

    Two elegant models have been proposed to explain the origin of the flower from an ancient bisexual strobilus (Baum and Hileman 2006, Theißen and Melzer 2007, Melzer et al. 2010), which cast doubt on earlier hypotheses from the standpoint of evo-devo of fertile SAMs.

    Stachyosporous origin hypotheses. David Winship Taylor and Kirchner (page 128, 1996) assert that, "... open carpels are a teratology and are not homologous with ancestral conduplicate carpels." I disagree with this proposal as it conflicts with earlier ideas expressed by Mamay (1976) and the reanalysis of Phasmatocycas bridwellii megasporophylls by Axsmith et al. (2003).

    A stachyosporous origin hypothesis better explains transformational series from ancestral glossopteridalean fertiligers to Mesozoic ovule-bearing cupules of Caytoniales, Corystospermales, Peltaspermales, and Petriellales, and not angiosperm carpels as argued by D. W. Taylor and Kirchner (1996).

    Seed fern hypotheses. James Doyle's seed fern hypotheses (1978, 2006) that develop an earlier proposal by Hamshaw Thomas (1925) on evolution of the angiosperm carpel and ovule integuments from Caytonia cupules, and Sergei Meyen's gamoheterotophic hypothesis (Meyen 1986, 1988) are difficult to explain by modern evo-devo models of floral origin involving cis-acting homeotic TFs.

    Carefully researched evo-devo proposals on the origin of the angiosperm outer integument from pteridosperm cupules involving transcriptional regulation of KANADI and YABBY outlined by J. A. Doyle (2006) on pages 175 and 176 of his review, are recently discussed within the context of studies of basal angiosperms (Endress 2011).

    Ovular and integumentary TFs such as KANADI and YABBY act downstream of CRMs underpinned by SAM maintenance- and floral meristem organ identity and integrator genes. Further, it may be impossible to extrapolate to extinct seed plants, the gene duplication, isoform genesis, subfunctionalization, and/or neofunctionalization events that might have occurred in deep time within and between these gene families.

    Frohlich and Parker's Mostly Male Theory (MMT) on ectopic ovules derived from male organs (2000) and later critiques of MMT based on paleontology of corystosperms and molecular evolution of cis-acting FLO/LFY homeotic selector genes (Frohlich 2002, 2003) are challenged by gene expression data of FLO/LFY homologs in female conifer cones and fertile SAMs (Vásquez-Lobo et al. 2007).

    Developmental evolutionary studies of pteridosperms including Corystospermales are impossible to conduct since this line of evolution died-out during the Paleogene Period of the Tertiary Interval (McLoughlin et al. 2008).

    Ophioglossoid origin hypothesis. Insight on alternative explanations for evolution of the carpel may be found in papers published by Kato (1990, 1991) on the anatomy and morphology of eusporangiate ferns.

    Kato developed a proposal on a neotenous origin of the carpel from Paleozoic glossopterid fertiligers based upon morphological studies of extant Ophioglossales (Kato 1988), an early divergent order of monilophytes. Figure 1 on page 190 of Kato (1991) outlines evolutionary steps in the "ophioglossoid model for angiosperm carpel archetype."

    Morphological-based proposals by Kato (1988, 1990, 1991) and Kato et al. (1988) namely, that Ophioglossales might represent living offshoots of early divergent homosporous, eusporangiate Devonian progymnosperms, are not supported by a detailed anatomical study of the Botrychium SAM (Rothwell and Karrfalt 2008).

    When in geologic time do molecular systematists and pteridologists pin-point the monilophyte and seed plant split?

    Pryer and coworkers (page 1586, 2004) estimate that "... initial divergence among monilophyte lineages ..." from seed plants occurred more than 360 MYA during late Devonian time. Whisk fern and ophioglossoids, "... diverged from one another in the Late Carboniferous ...", more than 300 MYA.

    Ferns and fern allies (monilophytes) potentially carry out development of fertile structures differently than extant seed plants based on biochemical and molecular phylogenetic studies of MIKC-type MADS-Box and FLO/LFY homeotic selector genes (Becker et al. 2000, Theißen et al. 2000, Hasebe et al. 2001, Himi et al. 2001).

    Pryer et al. (2004) state:

    "One of our remaining challenges will be to identify the Carboniferous ancestors of the whisk fern + ophioglossoid lineage."

    The preceding passage is quoted from page 1594 of Pryer et al. (2004), Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91(10): 1582-1598.

    Additional evo-devo research on ophioglossoid model monilophytes at the level of homeotic gene expression and homeodomain protein trafficking in meristematic tissues is needed. The leptosporangiate fern model organism Ceratopteris richardsonii is probably unsuitable for this purpose.

    Fertiliger (glossopterid) origin hypotheses. Evolutionary development of pteridosperm cupules and fertiligers (Schopf 1976, Retallack and Dilcher 1981, Melville 1983) is open to alternative explanations (Pigg and Trivett 1994).

    Ronald Melville's review on a Permian origin of angiosperms from glossopterids (1983) is a foundation for the homology assessment of fertiligers and carpels and a discussion of the gonophyll hypothesis.

    Stamen homologies. An evaluation of the origin, evolution, and homologies of the angiosperm stamen and associated structures is published by Crepet and Nixon (1996), Endress (1996), Hufford (1996), and Ronse De Craene and Smets (2001). Additional resources include Endress and Hufford (1989) and Hickey and D. W. Taylor (1996).

    There are two lines of reasoning on the homology of the stamen of flowering plants. Certain workers view the angiosperm stamen as fused tips of microsporangium-bearing branches of a telomb (see Stebbins 1974).

    The prevailing view of Canright (1952) is that pollen bearing organs of Degeneriaceae are microsporophylls (see Takhtajan 1969). "The laminar, spirally arranged androecium of Degeneriaceae is probably the most plesiomorphic trait of any extant flowering plant" (page 223, J. M. Miller 1989).

    A microsporophyll of Degeneria (Degeneriaceae, Magnoliidae) is imaged on the right side of the page, above. In my opinion, the microsporophyll of Degeneria is homologous with the laminar microsporophyll imaged in the earlier section on Phasmatocycas, and is not an anther as suggested by Endress and Hufford (1989) and Hufford (1996).

    Elongate rice-shaped structures on the adaxial leaf surface of the fossil illustrated in the chapter on gigantopterids (see Phasmatocycas section) may be microsporangia. I found this Permian (Leonardian) fossil in the same bedding plane as leaves of Delnortea abbottiae in 1981.

    The anatomy of the Phasmatocycas permineralization has not been studied. Its taxonomic affinities are unknown pending recovery of more material from the delnortea beds needed to demonstrate vascular connections with the mother plant.

    Pollen homologies. Ultrastructural details of pollen permineralizations are of importance in phylogenetic analyses of seed plants and pin-pointing the time and place of flowering plant origins. Considerable importance is placed on the anatomy and homology of pollen ultrastructural characters (J. A. Doyle 2009, Tekleva and Krassilov 2009).

    Angiospermous infratectal pollen structures (columellae and alveolae) and character variations of the nexine and tectum resembling both modern and fossil conifers and flowering plants, are known from permineralizations recovered from Permian rocks (Zavialova and Gomankov 2009). A discussion of these characters and their homologies is reserved for a later date.

    Homologies of the angiosperm ovule. Ovules of flowering plants are composed of the embryo sac (megagametophyte), a nucellus (old megasporangium wall), and sterile integuments. Integuments are generally regarded as modified leaves. Many but not all angiosperms possess two integuments. Understanding the evo-devo of ovular integuments (Skinner et al. 2004, Kelley et al. 2009, Endress 2011) is a prerequisite to understanding certain character homologies.

    Considerable attention has been paid to the evolution of tissue layers (integuments) of angiosperm ovules, which is intertwined with the evo-devo of fertile leaves and shoots. Reviews by Friedman et al. (2004), J. A. Doyle (2006), Kelley et al. (2009), and Endress (2011) are important starting points for this discussion.

    Preintegumentary lobes and cupulate systems enclosed the seeds of primitive Devonian seed plants (Serbet and Rothwell 1992), and these structures were enveloped by dichotomously-lobed non-foliar cupulate systems (also termed "cupules") that probably functioned in protection of ovules and seeds (T. N. Taylor et al. 2009).

    Thomas N. Taylor et al. (2009) do not regard Devonian seed plant cupulate systems as homologous with either megasporophylls of Paleozoic glossopterids or cupules of Mesozoic corystosperms and Caytoniales. I concur.

    Frohlich (2003) offers additional discussion on the origin of ovule integumentation from Mesozoic pteridosperms, and evo-devo of leaves and ovules from the standpoint of YABBY signaling from SAMs. But YABBY and KNOTTED1 homeodomain protein movement in the cells of SAMs might have been constrained by other factors such as distance of the fertile organ cell fields from the nuclear genes being activated.

    James Doyle discusses YABBY within the context of ovule tissue layers and attachment point (abaxial or adaxial) to carpels and leaves in Amborella, a basalmost angiosperm (J. A. Doyle 2006).

    Kelley et al. (2009) conclude that there are similarities between expression and transcriptional regulation of Class III HD-Zip, KANADI, and YABBY genes of integuments and leaves Arabidopsis (Brassicaceae, Brassicales, Rosanae). Based on biochemical studies of ovule polarity determinants, these workers state:

    "Although these organs [integuments and leaves] have distinct evolutionary origins, a common set of polarity determinants appears to have been serially utilized in both sets of structures. The differences in the precise roles and interactions of the determinants of each structure may represent differences dating from their origin, or alternatively, differences arising from subsequent structural diversifications."

    This quote is from page 1062 of D. K. Kelley, D. J. Skinner, and C. S. Gasser (2009), Roles of polarity determinants in ovule development. The Plant Journal 57(6): 1054-1064. The phrase in brackets [] is mine.

    Evolutionary development of the angiosperm outer integument and its supposed homology with reproductive structures of corystosperms suggested by Frohlich (2003) and Caytoniales proposed by J. A. Doyle (2006), may be explained differently (Kelley et al. 2009, Rudall et al. 2011).

    For example, tissue layering of ovular integuments of flowering plants may be a consequence of splitting of cell fields, which are derived from the inner integument and not a subtending foliar organ (Skinner and Gasser 2009).

    In conclusion, 300 million year old WGDs in the phylogeny of Class III HD-Zip genes (Floyd et al. 2006), and possibly YABBY, preclude derivation of the angiosperm carpel from any Mesozoic pteridosperm foliar organ.

    Seed plant/progymnosperm phylogenetic analyses. I conducted two separate sample phylogenetic analyses of gigantopteroid data based on the biological process homology concept, Process PTDSP and Process ANTHO. Two distinct biological processes of SAM homeotic TF and auxin/PIN protein trafficking are hypothesized in the MRCA at the time of WGDs that probably occurred during the late Devonian Period more than 350 MYA (Jiao et al. 2011).

    While students might choose available freeware such as MESQUITE, PHYLIP, or TNT (and retail software such as MACLADE), I executed David L. Swofford's Phylogenetic Analysis Using Parsimony (PAUP) program, version 4.0b10 on a Windows machine, and a computed two separate phylogenies.

    Anatomical and morphological data are from Bold et al. (1980), Cronquist (1981), Crane (1985), Trivett and Rothwell (1985), Serbet and Rothwell (1992), Crane (1996), Rothwell et al. (1996), Naugolnykh (2001), Axsmith et al. (2003), Friedman et al. (2004), Mundry and Stützel (2004), Z.-Q. Wang (2004), X.-Q. Liu et al. (2006), E. L. Taylor et al. (2006), J. A. Doyle (2009), Rothwell et al. (2009), T. N. Taylor et al. (2009), and Tekleva and Krassilov (2009).

    Source references for specific characters are cited and discussed in each of the two analyses, below. Biomarker data are from D. W. Taylor et al. (2006).

    Commands used in PAUP input blocks were simple and employed the most basic assumptions. Heuristic search methods were used to process the NEXUS files with maximum optimality parsimony settings. Characters were all the "unord" type with the "MultTrees" option selected.

    Further, the number of possibly informative characters adopted in these cladistic exercises (fewer than 30) departs radically from published work of others (Nixon et al. 1994, Rothwell and Serbet 1994, J. A. Doyle 2006, Hilton and Bateman 2006, J. A. Doyle 2008, Rothwell et al. 2009) who analyzed more than twice the number of characters. It is just that there are too many gaps in the data on possibly critical seed plant groups (and too many question marks [?] in the matrixes) when a full complement of characters is used, including hypothetical process-level evo-devo characters.

    The first phylogenetic analysis of core pteridosperms, Process PTDSP, is rooted with Aneurophyton (Aneurophytales) as the outgroup, and also includes Archaeopteris (Archaeopteridales), which are homosporous Devonian progymnosperms regarded by some paleobotanists as the Paleozoic ancestors of ferns and seed plants (T. N. Taylor et al. 2009).

    Spermatophytes scored in the Process PTDSP study are Autunia (Peltaspermales), Callistophyton (Callistophytales), Cycadales, Lyginopteris (Lyginopteridales), Elkinsia (Lyginopteridales), medullosans (lumped together to follow J. A. Doyle 2006), Peltaspermum (Peltaspermales), Petriella (Petriellales), and the cupule- and fertiliger-generating pteridosperms classified in the orders Caytoniales, Corystospermales, and Glossopteridales.

    A second analysis, Process ANTHO (including conifers) is rooted with Cycadales as the outgroup, and incorporates only those seed plant groups possessing simple and/or compound strobili (or in the case of female Ginkgo, which has no strobilus): angiosperms, Bennettitales, Coniferales, Czekanowskiales, gigantopteroids with protoflowers, Ginkgoales, Gnetales, Pentoxylales, Vojnovskyales, and conifers, among other key taxa (see character analysis Process ANTHO and Table 5).

    I left out some seed plant groups from these rudimentary phylogenetic analyses (e.g. Erdtmanithecales [including the taxa of charcoalified seeds, Friis et al. 2005 and 2006, Rothwell et al. 2009], Hermanophytales, Iraniales) but reserve the right to incorporate them into future revisions.

    Students and researchers alike are challenged to apply Cracraft's concept of historical-phylogenetic homology to evo-devo data (page 349, 2005) with added precision given to use of the concepts of "homocracy, homotopy, neofunctionalization, orthology, paralogy, and subfunctionalization" (page 211, Theißen 2005).

    Character analyses are generally patterned along the lines of published work by Nixon et al. (1994), Rothwell and Serbet (1994), J. A. Doyle (1996), Hickey and D. W. Taylor (1996), J. A. Doyle (2006), Hilton and Bateman (2006), and J. A. Doyle (2008) while incorporating Devonian pteridosperms in the analyses, but differ in one critical respect: two distinct groups of Paleozoic seed plants (cupule- and fertiliger-generating pteridosperms and strobilus-generating anthophytes + gigantopteroids) are analyzed separately.

    I will discuss the latest seed plant phylogenetic analysis by Rothwell et al. (2009) at a later date.

    Further, not all characters used in the Process PTDSP analysis were appropriate to incorporate into the Process ANTHO study and vice versa. I employed a basic set of 23 to 27 characters for each of the two phylogenetic analyses for two reasons: one, absence of data (principally glaring gaps in data on reproductive characters) on poorly studied extinct taxa precluded use of potentially informative traits, and two, simplicity of the analysis is concordant with my lingering doubts on some character homologies in deep time.

    Some of the ideas expressed herein might be justifiable on evo-devo grounds based on insight gained from molecular phylogenetic and biochemical studies of extant model vascular plant organisms and regulatory models of homeodomain proteins and cis-acting homeotic TFs (discussed in the previous section). Focused cladistic experiments may be included in future revisions of the analyses. More experimental data from evo-devo studies of a wider range of model extant lignophytes- and additional paleontological data are needed to shed light on anatomical and morphological homologies.

    Based on the discussion in the preceding section, I conclude that two different evo-devo programs: Process PTDSP for core pteridosperms without anthophytes + gigantopteroids, and another termed Process ANTHO for anthophytes + gigantopteroids, might have existed in Paleozoic vascular plants.

    Logically, vegetative and reproductive organs, e.g. leaves and sporophylls, of Process PTDSP pteridosperms and Process ANTHO seed plants might share no homology because these organs might be products of two different evo-devo programs downstream of SAM patterning genes and TFs.

    It is possible and even likely that an evo-devo dichotomy triggered the early round of WGDs predicted by Jiao et al. (2011) developed in races of Devonian seed plants leading to at least two modes of SAM trafficking of homeodomain proteins, and divergence in the anatomy and morphology of reproductive organs.

    More research is needed to refine the timing of WGDs estimated by Jiao et al. (2011) with fossil calibrations and tool kit data, either proving or disproving a Process PTDSP and Process ANTHO split.

    If the suggested molecular phylogenetic tool kit approach is proven correct, pteridosperms might not constitute "the backbone of seed-plant phylogeny" (title, Hilton and Bateman 2006), but may instead constitute a loose, paraphyletic group derived from Devonian ancestral seed plant stock.

    Process PTDSP and ANTHO character scoring and justifications, sample data sets, and matrixes are presented below.

    Core pteridosperms, progymnosperms, and cycads without anthophytes, conifers, and gigantopteroids: character analysis Process PTDSP. A numerical list of key seed plant characters with additional discussion appears below.

    1A. General plant habit. Woody shrubs, vines, or trees possessing secondary growth = 0; herbs usually with little or no secondary growth = 1.

    I scored this character the same way as J. A. Doyle (Appendix, Taxa and Characters, page S26, 1996) character 1; J. A. Doyle (Appendix 1, page 202, 2006) character 1; Hilton and Bateman (Appendix 2, page 160, 2006) character 2; and Nixon et al. (Appendix A, page 524, 1994) character 0. Arguments posed by Hickey and D. W. Taylor (1996) are inconsistent with evo-devo models of SAM organization in ferns.

    2A. General plant architecture. Long shoots present, short (spur) shoots absent = 0; both long and short (spur) shoots present = 1.

    Inclusion and polarity assignment of this character is in line with J. A. Doyle (Appendix, Taxa and Characters, page S26, 1996) character 4; Nixon et al. (Appendix A, page 525, 1994) character 2.

    3A. Stelar anatomy. Protostelic = 0; eustelic = 1; polystelic = 2.

    Nixon et al. adopted this character (Appendix A, page 525, 1994) character 4.

    4A. Apical meristem layering. Tunica absent = 0; tunica present, consisting of a single layer = 1.

    5A. Secondary tissues: wood. Manoxylic = 0; pycnoxylic = 1.

    Nixon et al. incorporated the wood character in their analysis (Appendix A, page 526, 1994) character 9.

    6A. Secondary tissues: rays. Uniseriate or biseriate = 0; multiseriate = 1.

    This character was included by Hickey and D. W. Taylor [Table 8.3, page 219, 1996] character 15; Nixon et al. (Appendix A, page 526, 1994) character 11.

    Polarity of the ray parenchyma character is reversed from J. A. Doyle (Appendix, Taxa and Characters, page S28, 1996) character 24, which is now consistent with a recent report of early Devonian secondary xylem having uniseriate rays (Gerrienne et al. 2011).

    7A. Leaf traces (nodal anatomy). One trace per leaf, unilacunar = 0; one trace per bundle = 1; trilacunar = 2.

    Considerable discussion and several variations on the scoring of this complex trait have been published (J. A. Doyle [Appendix, Taxa and Characters, page S28, 1996] character 17; J. A. Doyle [Appendix 1, page 203, 2006) character 23; J. A. Doyle [Appendix, 2008] character 28; Hilton and Bateman [Appendix 2, page 161, 2006] character 20; Nixon et al. [Appendix A, page 525, 1994] character 5; Rothwell and Serbet [Appendix 1, page 473, 1994] character 17).

    8A. Leaf venation (vegetative leaves). Open and dichotomous = 0; reticulate and anastomose = 1.

    Scoring of the leaf venation character agrees with J. A. Doyle (Appendix, Taxa and Characters, page S27, 1996) character 8; J. A. Doyle (Appendix 1, page 203, 2006) character 31; J. A. Doyle (Appendix, 2008) character 36; Rothwell and Serbet (Appendix 1, page 473, 1994) character 9, and is consistent with my hypothesis that a fundamental dichotomy in the process of homeodomain TF movement may exist in the evo-devo of seed plant SAMs.

    Adoption of multiple character states for vegetative leaf venation by Hickey and D. W. Taylor (Table 8.3, page 219, 1996) character 7, was considered for the Process PTDSP analysis, but rejected.

    9A. Leaves (vegetative). Pinnately compound = 0; simple and pinnate or pinnately-lobed = 1; simple and palmately-lobed or compound palmate = 2.

    10A. Stomata. Haplocheilic = 0; dicyclic stomatal complexes = 1.

    A new advanced stomatal character state is adopted for the Process PTDSP analysis based information from page 627 and page 629 of T. N. Taylor et al. (Figure 15.24, 2009), and knowledge that syndetocheilic stomata are not known from the Process PTDSP study taxa.

    Further, leaf epidermal traits in taxa within the Process PTDSP line of pteridosperm evolution such as dicyclic stomatal complexes might share no homology with syndetocheilic stomata of angiophytes. This line of deductive reasoning follows my hypothesis that a fundamental dichotomy in TF traffic patterns might exist in SAM development of Devonian seed plants possibly extending to downstream leaf epidermal patterning.

    11A. Reproductive life cycle attributes Homosporous = 0; heterosporous = 1.

    Choice and polarity assignment of aspects of the lignophyte reproductive life cycle is in line with Rothwell and Serbet (Appendix 1, page 473, 1994) character 1.

    12A. Ovulate axes (or equivalent eusporangiate axes). Eusporangia clustered on terminal shoots, or ovules aggregated and sheathed by cupulate axes on leafless shoots = 0; ovules aggregated or solitary on ectopic shoots arising from laminar leaf midribs, or sessile or nearly so on laminar megasporophylls aggregated into simple cones or not = 1; ovules sessile or nearly so and enclosed by a cupular leaf (cupule) = 2; ovules sessile or nearly so and attached to a peltate leaf = 3.

    13A. Microsporangiate axes (or equivalent eusporangiate axes). Eusporangial clusters, or microsporangia terminal on leafless shoots = 0; microsporangia clustered or fused on ectopic shoots attached to midribs of laminar microsporophylls aggregated into simple cones or not = 1; microsporangia clustered in synangia, sessile on pinnate leaves = 2.

    14A. Microsporangia (or equivalent eusporangial clusters) attachment to axes or leaves. Terminal = 0; abaxial = 1; adaxial = 2.

    James A. Doyle (Appendix 1, page 204, 2006) adopted this multistate character but added a fourth state (no. 49, lateral = 3), which I did not adopt.

    15A. Pollen (or equivalent pre-pollen) shape. Spores or pre-pollen radial = 0; pollen bilateral = 1; pollen global = 2.

    This character was employed by J. A. Doyle (Appendix 1, page 205, 2006) character 62; J. A. Doyle (Appendix, 2008) character 69; and Hilton and Bateman (Appendix 2, page 163, 2006) character 80, in their cladistic analyses of progymnosperms and spermatophytes.

    16A. Megasporophylls (or equivalent): ovule number per cupule, laminar megasporophyll, or peltate leaf. One (rarely two) ovule = 0; three to many ovules (rarely two) = 1.

    I scored ovule number along the lines of Nixon et al. (Appendix A, page 531, 1994) character 68.

    Petriella (Petriellales) was difficult to score for this character. Most Petriella fossils contain three to six ovules per cupule, so a "1" was scored (pages 637-639, T. N. Taylor et al. 2009).

    Uniovulate and strobilate Kannaskoppiaceae (pages 638-639, T. N. Taylor et al. 2009) are excluded from the analysis but may be included at a later date to better evaluate their character homologies and phylogenetic position.

    Restudy of the Caytonia cupule by scanning electron microscopy (Nixon et al. 1994) reveals that this structure may be a megasporophyll homologue (Hilton and Bateman 2006). This notion is called into question by Xin Wang (2010).

    There is no convincing paleobotanical evidence for past elegant proposals on the evo-devo of the angiosperm outer ovular integument and carpels from cupules and axillary organs of Mesozoic Caytoniales reviewed by Endress (2011), especially when the fast moving literature on molecular tool kits and ovular TFs (Kelley et al. 2009, Skinner and Gasser 2009, R. H. Brown et al. 2010, Tavares et al. 2010) is considered.

    Simply put, cone and floral tool kits are too conserved, possibly developing in several late Paleozoic gymnosperm populations, to somehow accommodate bizarre morphologies seen in Mesozoic Caytoniales within a logical chronocline leading to the Amborellanae, Nymphaeanae, and Magnolianae.

    This character is difficult to score for early Devonian seed plants since a lobed (dichotomous) non-foliar cupular system occurs in place of an ovule-bearing leaf (megasporophyll). Paleozoic progymnosperm seeds (e.g. Elkinsia), which are enclosed by a cupular system, were scored as "0."

    Dichotomously-lobed, non-foliar cupulate systems have been termed "cupules" in the literature on Devonian seeds (page 511, T. N. Taylor et al. 2009), but these authors do not view cupulate systems as homologous with either megasporophylls of glossopterids or cupules of corystosperms and Caytoniales.

    Callistophyton (Callistophytales) is one of the best known Paleozoic seed plants but details of ovule number per megasporophyll are problematic.

    17A. Megasporophylls (or equivalent): position of ovule attachment. Terminal = 0; marginal or adaxial = 1; abaxial = 2.

    Traditional ideas and supposed homologies of characters such as position of ovules on the megasporophyll, whether adaxial or abaxial (Figures 13 and 14, J. A. Doyle 2006), are called into question. I regard abaxial ovule attachment to the megasporophyll as the most derived character state in the Process PTDSP analysis, which is concordant with my suggestion that a wholly different evo-devo program of SAM transcriptional regulation and homeodomain protein trafficking occurred in this evolutionary line.

    Position of ovule attachment on the Callistophyton (Callistophytales) megasporophyll is unclear but detached leaves of the morphotype genus Pseudomariopteris bearing Callospermarion-like ovules are known (page 595, T. N. Taylor et al. 2009). Based on this circumstantial evidence I scored a "?" for character 17A.

    Several Paleozoic spermopteroid megasporophylls (see ANTHO analysis in next section) are known including Eophyllogonium cathayense (Mei et al. 1992), Phasmatocycas bridwellii (Axsmith et al. 2003), and Sobernheimia jonkeri (Kerp 1983; pages 709-711, T. N. Taylor et al. 2009). All of these possess stalked ovules attached to the abaxial surface of the megasporophylls, which is in contrast to marginal (to adaxial) ovule position on megasporophylls of true cycads (e.g. Crossozamia and Beania).

    Caytoniales and Dicroidium odontopteroides (Corystospermales) both possessed megasporophylls with ovules attached to the lower leaf surfaces, which is in agreement with Retallack and Dilcher (1988) and T. N. Taylor et al. (2009). Xin Wang in a recent provocative paleobotanical study (2010) suggests that cupule-bearing organs of Paracaytonia hongtaoi (Caytoniales) are parts of branches and not leaves.

    This is a major departure from J. A. Doyle (page 194, 2006) that also call into question some traditional ideas on Caytoniales and the origin of flowering plants published by Hamshaw Thomas (1925) and J. A. Doyle (1978).

    Simply put, if Caytonia and Dicroidium SAM tool kits were radically different from anthophytes than many supposed homologies of pteridosperm reproductive organs with angiosperm floral structures are completely incorrect.

    18A. Ovules (or equivalent eusporangium): position of attachment to axes or leaves. Erect = 0; inverted = 1.

    Choice and polarity assignment of ovule orientation is in line with J. A. Doyle (Appendix, Taxa and Characters, page S30, 1996) character 32; and Rothwell and Serbet (Appendix 1, page 474, 1994) character 29.

    Details of ovule attachment to the megasporophyll of Callistophyton (Callistophytales) are unclear. Based on this uncertainty I scored a "?" for character 18A.

    19A. Ovule: integuments (or equivalent). Ovule (preovule) enclosed by preintegumentary lobes, or lobed integuments partially fused with the megasporangium = 0; ovule enclosed by one or more integuments = 1.

    Preintegumentary lobes and cupulate systems enclosed the seeds of primitive Devonian seed plants (Serbet and Rothwell 1992), and these structures were enveloped by dichotomously-lobed non-foliar cupulate systems (also termed "cupules") that probably functioned in protection of ovules and seeds (T. N. Taylor et al. 2009).

    20A. Megasporangium (nucellus, or equivalent). With a lagenostome = 0; with a pollen chamber = 1.

    Choice and polarity assignment of this character is in line with J. A. Doyle (Appendix, Taxa and Characters, page S32, 1996) character 56; and Nixon et al. (Appendix A, page 532, 1994) character 75.

    21A. Megagametophytes. Archegonia present = 0; archegonia absent = 1.

    Many previous seed plant phylogenetic analyses (Hickey and D. W. Taylor [Table 8.3, page 221, 1996] character 49; Nixon et al. [Appendix A, page 533, 1994] character 86; Rothwell and Serbet [Appendix 1, page 476, 1994] character 60) include this organ (sometimes with multistate scoring e.g. J. A. Doyle [Appendix, Taxa and Characters, page S35, 1996] character 81), with the notable exception of Hilton and Bateman (2006).

    22A. Sperm transfer. Zooidogamous = 0; siphonogamous = 1.

    There is no paleobotanical evidence of sperm transfer in extinct Cycadales. Scoring of this character is based on living plants (Bold 1980). Unsubstantiated data for Hydrospermales (Elkinsia) and Lyginopteridales are included in the character matrix to follow rationale published by J. A. Doyle (2006), which is in line with a discussion of hydrospermalean reproduction by T. N. Taylor et al. (Chapter 13, 2009).

    Inclusion and polarity assignment of this character is in line with J. A. Doyle (Appendix, Taxa and Characters, page S35, 1996) character 79; J. A. Doyle (Appendix 1, page 205, 2006) character 73; J. A. Doyle (Appendix, 2008) character 82; and Hilton and Bateman (Appendix 2, page 163, 2006) character 90.

    Character data matrix Process PTDSP. A zero [0] in a cell denotes an ancestral (plesiomorphic) character state. Apomorphic (derived) character states are denoted in the table by the numeral one [1]. Multistate characters used in the analysis are: zero [0] (most plesiomorphic), numeral one [1] (neither plesiomorphic or apomorphic), two [2] (apomorphic), and three [3] (most apomorphic). The question mark [?] is equivalent to unassigned or missing data.

    Several characters scored in the Process ANTHO study (see next section), e.g. companion cells, vessel elements, multilacunar nodal anatomy, modular female gametophytes, and double fertilization, were omitted from the Process PTDSP analysis as they do not occur in any known extinct progymnosperms and pteridosperms.

    Further, at least one character used in previous attempts to resolve seed plant phylogeny using morphological data, secretory structs, was left-off both analyses. I could find no logical homology argument to justify inclusion of the character despite its inclusion in several seed plant phylogenetic analyses (J. A. Doyle [Appendix, Taxa and Characters, page S29, 1996] character 27; J. A. Doyle [Appendix 1, page 203, 2006] character 20; J. A. Doyle [Appendix, 2008] character 24; Hilton and Bateman [Appendix 2, page 161, 2006] character 32; Nixon et al. [Appendix A, page 526, 1994] character 17; and Rothwell and Serbet [Appendix 1, page 473, 1994] character 22).

    Table 4 is a matrix of characters used in the PAUP input block for a preliminary phylogenetic reconstruction of progymnosperms, cycads, cupule- and fertiliger generating seed plants, and peltasperms (see below). The Devonian progymnosperm, Aneurophyton (Aneurophytales) is selected as the outgroup (ANE).

    Character matrices typically are set-up such that operational taxonomic units (OTUs) or Hennigian "semaphoronts" appear in rows with the character array as columns. The matrix of characters below is arranged for ease of visual presentation on the web page: students may simply rotate the block 90° for a conventional view.

    Additional lignophytes were also scored: Antarcticycas schopfii, including Delemaya spinulosa (Cycadales) = ANT, Archaeopteris (Archaeopteridales) = ARC, Autunia (Peltaspermales) = AUT, Lyginopteris (Lyginopteridales) = LYG, Callistophyton (Callistophytales) = CAL, Crossozamia (Cycadales) = CRO, Elkinsia (Hydrospermales), medullosans = MED, Peltaspermum (Peltaspermales) = PEL, and Petriella (Petriellales) = PET.

    Key extinct groups in the PAUP "TAXA Block" that possess cupules or, alternatively fertiligers (Table 4) are: Caytonia (Caytoniales) = CAY, Dicroidium (Corystospermales) = DIC including detached branches of cupules described as Umkomasia, and Glossopteris (Glossopteridales) = GLO.


    Table 4. Core Pteridosperms, Progymnosperms, and Cycads Without Anthophytes, Conifers, and Gigantopteroids: Character Data Matrix Process PTDSP.

    Char/Grp

    ANE

    ANT

    ARC

    AUT

    CAY

    CAL

    CRO

    DIC

    ELK

    GLO

    LYG

    MED

    PEL

    PET

    1A Habit

    0

    0

    0

    1

    ?

    0

    0

    0

    0

    0

    0

    0

    1

    ?

    2A Architecture

    0

    0

    0

    1

    ?

    0

    0

    1

    0

    1

    0

    1

    1

    ?

    3A Stele Anatomy

    0

    2

    1

    1

    ?

    1

    2

    2

    ?

    1

    1

    ?

    1

    ?

    4A Apical meristem

    0

    0

    0

    ?

    ?

    0

    0

    0

    0

    0

    0

    0

    ?

    ?

    5A Secndry Xylem

    0

    1

    1

    1

    ?

    1

    1

    1

    ?

    1

    1

    1

    1

    ?

    6A Ray Parenchyma

    0

    1

    1

    1

    ?

    1

    1

    1

    ?

    1

    0

    1

    1

    ?

    7A Leaf Traces

    0

    1

    1

    1

    ?

    1

    1

    1

    ?

    1

    1

    1

    1

    ?

    8A Leaf Venation

    0

    0

    0

    0

    1

    0

    0

    0

    0

    0

    0

    0

    0

    ?

    9A Leaves

    0

    0

    0

    0

    2

    0

    0

    0

    0

    1

    0

    0

    0

    ?

    10A Stomata

    0

    0

    0

    0

    1

    ?

    0

    0

    ?

    1

    0

    0

    0

    ?

    11A Life Cycle Attrib

    0

    1

    0

    1

    1

    1

    1

    1

    1

    1

    1

    1

    1

    1

    12A Ovulate/Euspgm Axes

    0

    1

    0

    3

    2

    1

    1

    1

    0

    1

    0

    0

    3

    2

    13A Microspgm/Euspgm Axes

    0

    1

    0

    2

    2

    1

    1

    1

    ?

    1

    1

    0

    2

    ?

    14A Microspgm/Euspgm

    0

    2

    0

    2

    2

    1

    2

    1

    ?

    1

    1

    1

    2

    ?

    15A Po/PrePo Shape

    0

    1

    0

    2

    2

    1

    1

    1

    ?

    1

    0

    0

    2

    ?

    16A Ov/Euspgm No/Sphyll

    0

    0

    0

    1

    1

    ?

    0

    1

    0

    1

    1

    0

    1

    1

    17A Ov/Euspgm Attach

    0

    1

    1

    2

    2

    ?

    1

    2

    0

    1

    1

    1

    2

    2

    18A Ov/Euspgm Posit

    0

    1

    0

    1

    1

    ?

    1

    1

    0

    1

    1

    0

    1

    1

    19A Integ or Equiv

    0

    1

    0

    1

    1

    1

    1

    1

    0

    1

    1

    0

    1

    1

    20A Megaspgm/Nuc

    0

    1

    0

    1

    1

    1

    1

    1

    1

    1

    1

    0

    1

    1

    21A MegaGpts

    0

    0

    0

    ?

    ?

    0

    0

    1

    0

    0

    0

    0

    ?

    ?

    22A Sperm Transfer

    ?

    0

    ?

    1

    ?

    ?

    0

    1

    0

    0

    0

    ?

    1

    ?


    Anthophytes, conifers, and gigantopteroids without core pteridosperms: character analysis Process ANTHO. A numerical list of key seed plant characters with detailed discussion and homology assessment (character analysis Process ANTHO) appears below.

    1B. General plant habit. Woody shrubs, vines, or trees possessing secondary growth = 0; herbs usually with little or no secondary growth = 1.

    Character scoring of plant habit is consistent with J. A. Doyle (Appendix, Taxa and Characters, page S26, 1996) character 1; J. A. Doyle (Appendix 1, page 202, 2006) character 1; Hilton and Bateman (Appendix 2, page 160, 2006) character 2; and Nixon et al. (Appendix A, page 524, 1994) character 0.

    Arguments posed by D. W. Taylor and Hickey (page 233, 1996) in their formulation of the "herbaceous origin hypothesis" (formerly known as the "paleoherb hypothesis") are rejected because they contradict a later proposal rolled-out by D. W. Taylor et al. (2006): namely, woody Paleozoic gigantopterids are in the same clade as bennettitaleans and flowering plants, based on leaf and stem anatomy and the distribution of oleanone triterpanes.

    I was unable to ascertain the general plant habit for the Czekanowskiales (Krassilov 1975, Krassilov 1997, X.-Q. Liu 2006) or Schmeissneria (gymnosperm incertae cedis, SN) from the description for Schmeissneria sinensis in X. Wang et al. (2007) or from T. N. Taylor et al. (page 753, 2009) so a "?" was entered in the data matrix for this character. Schmeissneria possesses both long- an short shoots suggesting a shrub-like habit.

    Paleozoic seed plants described by Neuburg in 1955 as Vojnovskya paradoxa (Vojnovskyales = VJ) possessed a shrub-like habit according to Mamay (1976). Secondary growth has been documented in permineralized stem fragments of Sergeia neuburgii recovered from Carboniferous marine turbidites but the plant architecture is unknown (Rothwell et al. 1996). I scored Vojnovskyales with a "0" based on Mamay's evaluation of Vojnovskya paradoxa and modified drawing of an earlier reconstruction of the plant (Text-Fig. 1, page 291, 1976).

    2B. Natural products biochemistry. Oleananes absent = 0; oleananes present = 1.

    Oleananes, together with ursenes, lupenes, and taraxerenes are important TSBs that belong to a class of Β-amirin triterpenoids (Moldowan and Jacobson 2002). Experimental studies and analyses conducted by D. W. Taylor et al. (2006) when viewed from a biosynthetic and phylogenetic perspective, validate the potential usefulness of this character in the ANTHO analysis.

    Class 1c terpenoids were components in Carboniferous gymnosperm amber (Bray and K. B. Anderson 2009). Inclusion of the resin biomarker character in the ANTHO analysis is warranted because of the potential importance of antiherbivory and antifungal agents in early angiosperm and conifer evolution.

    Oleonone triterpane data are needed for many critical taxa of seed plants. The conifer Araucaria was scored as a "0" based on the possibility that unidentified Cretaceous conifer wood in D. W. Taylor et al. (Table 1, page 184, 2006) belonged to this genus.

    3B. Xylary conducting elements. Tracheids present and vessels absent = 0; vessel elements present in addition to tracheids = 1.

    The character was scored to follow the lead of J. A. Doyle (Appendix, Taxa and Characters, page S28, 1996) character 22; Hickey and D. W. Taylor (Table 8.3, page 219, 1996) character 13; Hilton and Bateman (Appendix 2, page 161, 2006) character 25; Nixon et al. (Appendix A, page 526, 1994) character 12; and Rothwell and Serbet (Appendix 1, page 473, 1994) character 21.

    James A. Doyle (2006) subdivides this traditional xylem character into several discreet characters. I did not adopt this approach at the present time because of great gaps in the data.

    4B. Apical meristem layering. Tunica absent = 0; tunica present, consisting of a single layer = 1; tunica present, consisting of two layers = 2.

    5B. Phloem conducting elements. Companion cells absent = 0; companion cells present = 1.

    Scoring of this character conforms to J. A. Doyle (Appendix, Taxa and Characters, page S28, 1996) character 25; J. A. Doyle (Appendix 1, page 203, 2006) character 17; J. A. Doyle (Appendix, 2008) character 19; Hilton and Bateman (Appendix 2, page 161, 2006) character 29; and Nixon et al. (Appendix A, page 526, 1994) character 15.

    I did not include characters of phloem tissue in the PTDSP study, since companion cells are not known from any of the taxa studied in that grouping of progymnosperms and seed plants.

    6B. Secondary tissues: wood. Manoxylic = 0; pycnoxylic = 1; absent or nearly so = 2.

    Nixon et al. incorporated the wood character in their analysis (Appendix A, page 526, 1994) character 9.

    The bizarre morphology of Welwitschia mirabilis (Gnetales, WW) complicates scoring of secondary growth characters for the species (Carlquist 1996). Based on Carlquist's paper I decided to score Welwitschia mirabilis with a "1" for both traits pertaining to secondary growth.

    7B. Secondary tissues: rays. Uniseriate or biseriate = 0; multiseriate = 1; absent or nearly so = 2.

    This character was included by Hickey and D. W. Taylor (Table 8.3, page 219, 1996) character 15; Nixon et al. (Appendix A, page 526, 1994) character 11.

    James A. Doyle (Appendix, Taxa and Characters, page S28, 1996) character 24, reverses the polarity of the ray parenchyma trait. I disagree with J. A. Doyle's polarity reversal of this character. My opinion is based on a study by Gerrienne et al. (2011) who report uniseriate rays in secondary xylem of stems in some of the oldest lignophytes unearthed from Devonian rocks.

    8B. Leaf traces (nodal anatomy). One trace per leaf, unilacunar = 0; one trace per bundle = 1; multilacunar or trilacunar = 2.

    I departed from J. A. Doyle (Appendix, Taxa and Characters, page S28, 1996) character 17, in describing various states of this trait.

    9B. Leaf venation of vegetative leaves born on long shoots. Dichotomose, simple, or parallel veins, one or two orders of venation, terminal veins open = 0; reticulate or parallel, one or more orders of venation, terminal veins anastomose = 1, reticulate with three or more orders, terminal veins anastomose = 2.

    Hickey and D. W. Taylor (Table 8.3, page 219, 1996) character 7 is similar.

    Heteroblastic andropetals, microsporophylls, and megasporophylls of fertile spur shoots of the same Evolsonia-like gigantopteroid mother plant might have resembled some retuse Taeniopteris morphotypes or even Lonesomia mexicana, which is a profound departure from traditional views on Paleozoic gymnosperm (anthophyte) whole plant morphologies.

    10B. Leaves (vegetative). Compound- pinnate = 0; simple- palmate, pinnate, needle-like, or scale-like = 1; compound- palmate, dissected, or palmately-lobed = 2.

    Polarization of the vegetative leaf character agrees, in part, with J. A. Doyle (Appendix, Taxa and Characters, page S27, 1996) character 6, which is similar to Hilton and Bateman (Appendix 2, page 160, 2006) character 7.

    Nixon et al. (Appendix A, page 527, 1994) character 24 treat leaf morphology as a binary character, scoring simple leaves as the plesiomorphic state and compound leaves as derived. I disagree.

    Experimental manipulation of an extant pinnate-leaved cycad model organism by introducing a WGD or Class III HD-Zip gene duplication might shed light on whole leaf developmental homologies.

    I regarded the pinnate vegetative leaves of Paleozoic Yuania and Tianbaolinia morphotypes of Crossozamia cycads as the plesiomorphic condition (note my discussion of Paleozoic gigantopteroid simple megasporophylls, below).

    11B. Stomata. Haplocheilic = 0; syndetocheilic = 1.

    Scoring of the stomatal character state is consistent with J. A. Doyle (Appendix, Taxa and Characters, page S27, 1996) character 11; Nixon et al. (Appendix A, page 528, 1994) character 32; and Rothwell and Serbet (Appendix 1, page 473, 1994) character 12.

    Derived leaf epidermal traits (syndetocheilic stomata) in taxa within the Process ANTHO line of seed plant evolution are probably not homologous with advanced dicyclic stomatal complexes of the Process PTDSP evolutionary line. This proposal is consistent with my hypothesis that a fundamental dichotomy in homeodomain TF trafficking might exist in SAM development of seed plants possibly extending to downstream leaf epidermal patterning TFs.

    12B. Sporophylls (with aggregations of sporangia). Clustered together in massive hermaphroditic (bisexual) strobili (cones) = 0; clustered together in reduced hermaphroditic (bisexual) strobili (cones) = 1; clustered together in reduced hermaphroditic (bisexual) flowers = 2; flowers reduced to unisexual flowers or non-flowers = 3.

    A detailed homology assessment of Process ANTHO fertile structures, which are proposed herein as products of a distinct evo-devo of SAM organization is discussed in the preceding sections. Carpels of flowers are therefore, homologous with gigantopteroid (Phasmatocycas bridwellii) megasporophylls of simple but massive proanthostrobili.

    Assignment of the plesiomorphic (ancestral) character state to massive hermaphroditic (bisexual) strobili posits that 300 million year old Paleozoic gigantopteroids possessed flower-like proanthostrobili. Extant conifer and gnetalean cones and angiosperm flowers are considered here as apomorphic (shared-derived) products of neotenous evolution.

    13B. Strobilus (cone) and floral gender. Bisexual (hermaphroditic, monoecious) pollen-bearing (male, microsporangiate) and ovule-bearing (female, megasporangiate) = 0; unisexual (dioecious), either pollen-bearing (male, microsporangiate) or ovule-bearing (female, megasporangiate) = 1.

    Paleozoic cycads are known from both China and North America (Norstog and Nicholls 1997, L. Liu and Z. Yao 2002). Permian cycads include members of the genus Crossozamia (CR), which are known only from detached fossilized megasporophylls. A Carboniferous cycad species, Lasiostrobus polysaccii is known only from detached pollen cones.

    Extant cycads are dioecious. Therefore, it is not clear whether Paleozoic cycads existed as separate male and female plants, hence a "?" was scored for this character in the CR column.

    14B. Strobilus (cone) and floral organization. Simple, bisexual (simple pollen-bearing [male, microsporangiate] and simple ovule-bearing [female, megasporangiate]) proanthostrobilus = 0; simple, pollen-bearing (male, microsporangiate) and/or compound ovule-bearing (female, megasporangiate, bracteose) = 1; simple, pollen-bearing (male, microsporangiate) cones present or reduced to naked, stalked microsporangia at spur shoot apexes, and ovule-bearing (female, megasporangiate) pedicels at the apex of spur shoots, and/or ovules borne in clusters or singly subtended by a cupule-like collar = 2; neotenous reduction of the strobilus to bisexual flowers, unisexual flowers, or non-flowers = 3.

    Spermopteroid Paleozoic reproductive structures including Eophyllogonium cathayense (Mei et al. 1992), Phasmatocycas bridwellii (Axsmith et al. 2003), and Sobernheimia jonkeri (Kerp 1983; pages 709-711, T. N. Taylor et al. 2009) might be pieces of bisexual gigantopteroid proanthostrobili with the male parts missing (see discussion above), which are coded under "GI" in the matrix below.

    A great body of classical, evo-devo, and paleobotanical literature is devoted to the morphology of the proanthostrobilus, cone, and flower (Arber and Parkin 1907, Florin 1954, Takhtajan 1976, Baum and Hileman 2006, Theißen and Melzer 2007, T. N. Taylor et al. 2009, Melzer et al. 2010). Scoring of Mesozoic Ginkgoales and Pentoxylales is problematic since taxa in both orders deviate from classical and contemporary models of cone and floral evo-devo.

    Extinct Ginkgoales are well-documented from Mesozoic rocks of Asia and exhibit a transitional series (page 751, Figure 18.18, T. N. Taylor et al. 2009) in ovule-bearing (female) trees. Megasporophylls are reduced to cupule-like collars subtending ovules borne in clusters or singly. Megastrobili of Karkenia and Kerpia are therefore, missing laminar megasporophylls and consist of clustered, woody ovulate units (page 752, T. N. Taylor et al. 2009).

    Equally perplexing are ovulate clusters of Pentoxylales described as Carnoconites. Howe and Cantrill (2001) provide a detailed discussion of the homologies of Carnoconites ovule-bearing spur shoots, which are almost certainly evolutionarily reduced megastrobili lacking laminar megasporophylls.

    Pollen-bearing cones and microsporophylls of Pentoxylales are absent and reduced to naked, stalked microsporangia arising from spur shoot apexes (see Crane 1985 [Crane's illustration is reproduced earlier in this essay] and Figure 19.25 on page 771 of T. N. Taylor et al. 2009).

    Based upon current thinking on the phylogenetic relationships of Ginkgoales and Pentoxylales (T. N. Taylor et al. 2009), I view "strobilus (cone) and floral organization" as a multistate character while scoring these two enigmatic Mesozoic orders of Process ANTHO seed plants with a "2."

    Reinterpretation of the floral morphology of the Cretaceous crown eudicot Archaefructus by Friis et al. (2003) is reflected in the scoring of the floral organization trait, which is consistent with J. A. Doyle (2008).

    15B. Microsporophylls. Taeniopteroid with adaxial microsporangia = 0; net-veined with adaxial microsporangia or furrows = 1; microsporangia terminal on stalks at spur shoot apexes = 2; microsporangia adaxial or abaxial on ribbon-shaped stamens, or microsporangia fused in stamens variously modified often with a distinct filament and anther = 3.

    It was not possible to ascertain details of the microsporophyll and attached pollen sac (microsporangium) of Palaeognetaleana auspicia (Gnetales) due to poor preservation of the bisexual cone (Z.-Q. Wang 2004), so a "?" was scored for characteristics of the pollen sac-bearing cone scale.

    16B. Pollen. Monosulcate = 0; anasulcate, colpoporate = 1; tricolpate or polycolpate, pororate = 2.

    Choice and polarity assignment of this character follows Nixon et al. (Appendix A, page 529, 1994) character 47.

    17B. Pollen saccus. absent (non-saccate) = 0; present but rudimentary (sub-saccate) = 1; present and inflated = 2 (saccate).

    This multistate character deviates from J. A. Doyle (Appendix, Taxa and Characters, page S34, 1996) character 70; and Nixon et al. (Appendix A, page 529, 1994) character 47 to accommodate sub-saccate pollen of Vojnovskyales: a critical group of hermaphroditic Paleozoic seed plants neglected in almost all previous phylogenetic analyses.

    18B. Pollen ultrastructure (infratectal). Massive or spongy aveolar = 0, honeycomb aveolar = 1, granular and/or columellar = 2.

    I included J. A. Doyle's characters of the infratectum (2009), which is patterned the same way as his earlier analyses (J. A. Doyle [Appendix, Taxa and Characters, page S34, 1996] character 71; J. A. Doyle [Appendix 1, page 205, 2006] character 64; and J. A. Doyle (Appendix, 2008) character 72.

    Further discussion of pollen surface ornamentation, wall anatomy, and ultrastructure within the context of Paleozoic angiospermous and coniferous pollen characters is published by Zavialova and Gomankov (2009).

    19B. Pollen exine. Exine striations absent = 0; exine striations present = 1.

    This character was employed by J. A. Doyle (Appendix 1, page 205, 2006) character 65; J. A. Doyle (Appendix, 2008) character 73; and Hilton and Bateman (Appendix 2, page 163, 2006) character 83, in their cladistic analyses.

    20B. Microgametophytes. Multinucleate = 0, tetranucleate = 1, trinucleate = 2.

    Inclusion and polarity assignment of this character is in line with J. A. Doyle (Appendix, Taxa and Characters, page S35, 1996) character 77; Nixon et al. (Appendix A, page 530, 1994) character 56; and Rothwell and Serbet (Appendix 1, page 476, 1994) character 54.

    21B. Megasporophyll (or equivalent non-foliar cupular system, or modified pedicels at the apex of spur shoots, or conduplicately-folded megasporophyll [carpel]): ovule number. Ovules per megasporophyll, many = 0; ovules per megasporophyll, 1 or 2 = 1; ovules per conduplicately-folded megasporophyll (carpel), 1 to many = 2.

    I reversed the polarity assignment of this character from Nixon et al. (Appendix A, page 531, 1994) character 68, to conform with the idea expressed in the homology assessment discussed in a previous section. The gigantopteroid megasporophylls of Phasmatocycas bridwellii, which are possibly detached internal pieces of the innermost whorl of a much larger protoflower, and possessing many ovules attached to abaxial megasporophyll surfaces.

    22B. Megasporophyll (or equivalent non-foliar cupular system, or modified pedicels at the apex of spur shoots, or conduplicately-folded megasporophyll [carpel]): position of ovule attachment. Abaxial = 0; adaxial = 1.

    Abaxial (lower) attachment of ovules to the megasporophyll conforms with my homology assessment. Detached gigantopteroid megasporophylls of Phasmatocycas bridwellii possess ovules attached to the abaxial leaf surface, which is consistent with Axsmith et al. (2003).

    Based on the discussion in the preceding sections titled "Gigantopterids," "Phasmatocycas and other spermopterids," and "Hypothetical gigantopteroid protoflowers," I regard the ovule-bearing leaves of Eophyllogonium cathayense, Phasmatocycas bridwellii, and Sobernheimia jonkeri as detached pieces of enormous protoflowers, which are probably equivalent to J. A. Doyle's concept of "proanthostrobili."

    23B. Ovules: position. Erect = 0; inverted = 1.

    Choice and polarity assignment of ovule orientation is in line with J. A. Doyle (Appendix, Taxa and Characters, page S30, 1996) character 32; and Rothwell and Serbet (Appendix 1, page 474, 1994) character 29.

    24B. Ovules: integuments. Integument adnate with the megasporangium wall (nucellus) only at the base, or midway along the ovule axis, integument one-layered = 0; integument adnate to the nucellus, the integument consists of one or more layers (so-called double integuments probably form by simple splitting of tissue layers during ovule development) = 1.

    Ovular tissue layers external to the megasporangium wall (nucellus) are discussed by Rothwell and Serbet (1994). Polarity assignment is consistent with Rothwell and Serbet (Appendix 1, page 475, 1994) character 39.

    A full discussion of ovular integument homologies is discussed in a previous section. Based on this homology assessment and conflicting data from the study of ovule determinants in extant model eudicots, traditional ideas on the phylogenetic significance of the angiosperm double integument (J. A. Doyle 1978, 2006, Endress 2011) are rejected.

    There is no convincing paleobotanical evidence for past elegant proposals on the evo-devo of the angiosperm outer ovular integument and carpels from cupules and axillary organs of Mesozoic Caytoniales reviewed by Endress (2011), especially when the fast moving literature on molecular tool kits and ovular TFs (Kelley et al. 2009, Skinner and Gasser 2009, R. H. Brown et al. 2010, Tavares et al. 2010) is considered.

    Therefore integumentary layers (double integuments) probably form by simple splitting of tissue layers during ovule development.

    25B. Megasporangium (nucellus). Pollen chamber present at the apex of a multicellular megasporangium = 0; pollen chamber absent and megasporangium reduced to a nucellus = 1.

    26B. Megagametophytes. Archegonia present, female gametophyte tissue many-celled = 0; archegonia absent, female gametophyte tissue reduced to a few modular cells and nuclei = 1.

    27B. Sperm transfer. Zooidogamous = 0; siphonogamous = 1.

    There is no paleobotanical evidence of sperm transfer in extinct Cycadales. Scoring of this character is based on living plants (Bold 1980).

    Inclusion and polarity assignment of this character is in line with J. A. Doyle (Appendix, Taxa and Characters, page S35, 1996) character 79; J. A. Doyle (Appendix 1, page 205, 2006) character 73; J. A. Doyle (Appendix, 2008) character 82; and Hilton and Bateman (Appendix 2, page 163, 2006) character 90.

    28B. Fertilization. Single = 0; double = 1.

    This character was included by Hickey and D. W. Taylor (Table 8.3, page 222, 1996) character 52.

    I agree with Friedman and Carmichael's (1996) homology assessment of double fertilization in anthophytes.

    Character data matrix Process ANTHO. A zero [0] in a cell denotes an ancestral (plesiomorphic) character state. Apomorphic (derived) character states are denoted in the table by the numeral one [1]. Multistate characters used in the analysis are: zero [0] (most plesiomorphic), numeral one [1] (neither plesiomorphic or apomorphic), two [2] (apomorphic), and three [3] (most apomorphic). The question mark [?] is equivalent to unassigned or missing data.

    I selected Crossozamia (Cycadales) = CR, as the outgroup for the Process ANTHO analysis for several reasons:

  • (1) Crossozamia first appeared in the Permian Period (see T. N. Taylor et al. 2009) approximately coinciding with the interval in geologic time when the angiosperms split from the MRCA,
  • (2) Crepet and Niklas (2009) point out that polyploidy is absent in extant cycads, possibly reflecting an absence of WGDs in this Permo-Carboniferous lineage,
  • (3) Cycadales are basal to all angiophyte and coniferophyte seed plant taxa in a molecular constraints strict consensus tree (page 184, Figure 8, J. A. Doyle 2006), and
  • (4) cycads are basal in Hilton and Bateman's summary tree (page 150, Figure 16, 2006).
  • Spermopteroid Paleozoic seed plants Archaeocycas whitei (page 8, Mamay 1976), Eophyllogonium cathayense (Mei et al. 1992), Phasmatocycas bridwellii (Axsmith et al. 2003), and Sobernheimia jonkeri (page 713, Figure 17.23, T. N. Taylor et al. 2009) might be ovulate pieces of bisexual gigantopteroid protoflower with the male parts missing. I regard all four of these species as a whole new group of gigantopteroid Paleozoic seed plants, and do not include them in the Cycadales where T. N. Taylor et al. (pages 709-713, 2009) discusses them, which is in line with Axsmith et al. (2003).

    Since Callistophyton (Callistophytales) is one of the best known Paleozoic seed plants and possesses conifer-like pollen, I considered it as a potential outgroup for the ANTHO analysis. Yet, when compared with Crossozamia (Cycadales), position of ovule attachment to the megasporophyll of Callistophyton is conjectural. On this basis, Callistophyton was rejected as an outgroup for the ANTHO analysis.

    Table 5 is a matrix of seed plant characters used in the PAUP input block for a preliminary phylogenetic reconstruction of 20 seed plant taxa (see below).

    Character matrices typically are set-up such that operational taxonomic units (OTUs) or Hennigian "semaphoronts" appear in rows with the character array as columns. The matrix of characters below is arranged for ease of visual presentation on the web page: students may simply rotate the block 90° for a conventional view.

    AF = Archaefructus (a crown angiosperm eudicot), AM = Amborella trichopoda (a basal angiosperm), AR = Araucariaceae (Coniferales), BE = Bennettitales (including Cycadeoidea and Vardekloeftia), CO = Cordaitales, CZ = Czekanowskiales, and DG = Degeneria (a genus of magnoliid flowering plants).

    Additional seed plant taxa subjected to phylogenetic analysis (Table 5) are: EM = Emporia (Voltziales), GK = Ginkgoales, GN = Gnetum + all species combined (Gnetales), HY = Hydatellaceae (basal angiosperm family, formerly a commelinid monocot), MA = Magnoliaceae, including Liriodendron and Magnolia (Magnoliales), and NY = Nymphaeales (basal angiosperm order).

    Hypothetical gigantopteroids (GI) were scored from a combination of characters seen in detached organs of several Paleozoic gymnosperms (including gigantopterids and Phasmatocycas bridwellii) that may or may not be attached to the same mother plant: unknown protoflowers with whorls of heteroblastic tepals, Lonesomia mexicana-like andropetals, laminar taeniopteroid microsporophylls, and Phasmatocycas bridwellii-like megasporophylls; combined with leaf anatomical characters of Delnortea abbottiae and Evolsonia texana.

    Finally, I included PG = Palaeognetaleana (Gnetales), PE = Pentoxylon sahnii (Pentoxylales), SA = Sanmiguelia lewisii (gymnosperm incertae cedis), SN = Schmeissneria (gymnosperm incertae cedis), VJ = Vojnovskyales based on Paravojnovskya imbricata (but including characters from the other vojnovskyalean genera), and WW = Welwitschia mirabilis (Gnetales).


    Table 5. Anthophytes, Conifers, and Gigantopteroids without Core Pteridosperms: Character Data Matrix Process ANTHO.

    Char/Grp

    AF

    AM

    AR

    BE

    CO

    CR

    CZ

    DG

    EM

    GI

    GK

    GN

    HY

    MA

    NY

    PE

    PG

    SA

    SN

    VJ

    WW

    1B Habit

    1

    0

    0

    0

    0

    0

    ?

    0

    0

    0

    0

    0

    1

    0

    1

    0

    ?

    1

    ?

    0

    0

    2B NP Biochem

    ?

    ?

    0

    1

    0

    ?

    ?

    ?

    ?

    1

    ?

    0

    ?

    ?

    ?

    ?

    ?

    ?

    ?

    ?

    ?

    3B Xylem CEs

    ?

    0

    0

    0

    0

    0

    ?

    0

    0

    1

    0

    1

    1

    0

    0

    0

    ?

    ?

    ?

    0

    1

    4B Apical meristem

    ?

    ?

    0

    ?

    0

    0

    ?

    1

    ?

    ?

    0

    1

    ?

    1

    2

    ?

    ?

    ?

    ?

    ?

    ?

    5B Phloem CEs

    ?

    ?

    0

    0

    0

    0

    ?

    1

    0

    1

    0

    0

    1

    1

    1

    0

    ?

    ?

    ?

    0

    0

    6B Secndry Xylem

    ?

    1

    0

    0

    1

    0

    ?

    1

    1

    1

    1

    1

    2

    1

    2

    1

    ?

    ?

    ?

    ?

    1

    7B Ray Parenchyma

    ?

    1

    1

    0

    1

    0

    ?

    1

    1

    1

    1

    1

    2

    1

    2

    1

    ?

    ?

    ?

    ?

    1

    8B Leaf Traces

    ?

    2

    2

    1

    2

    1

    ?

    2

    1

    2

    2

    2

    2

    2

    2

    1

    ?

    ?

    ?

    ?

    2

    9B Leaf Venation

    1

    2

    1

    1

    2

    1

    0

    2

    1

    2

    0

    2

    1

    2

    2

    1

    ?

    1

    0

    0

    1

    10B Leaves

    1

    1

    1

    0

    1

    0

    2

    1

    1

    1

    2

    1

    1

    1

    1

    1

    ?

    1

    1

    1

    1

    11B Stomata

    1

    1

    0

    0

    0

    0

    1

    1

    1

    1

    0

    1

    1

    1

    0

    0

    ?

    1

    1

    1

    1

    12B Sphylls

    2

    0

    1

    1

    1

    1

    1

    0

    1

    0

    1

    1

    2

    0

    0

    1

    0

    0

    1

    0

    1

    13B Strobilus Sex

    0

    0

    1

    1

    1

    ?

    1

    0

    1

    0

    1

    1

    0

    0

    0

    1

    0

    0

    1

    0

    1

    14B Strobilus Org

    3

    3

    1

    0

    0

    0

    2

    3

    0

    0

    2

    1

    3

    3

    3

    2

    1

    3

    2

    0

    1

    15B MicroSphylls

    3

    3

    1

    0

    1

    0

    1

    1

    1

    0

    1

    3

    3

    3

    3

    2

    ?

    1

    1

    ?

    3

    16B Pollen Shape

    0

    0

    0

    0

    0

    0

    ?

    0

    0

    ?

    0

    0

    0

    0

    0

    1

    0

    1

    1

    ?

    0

    17B Pollen Saccus

    0

    0

    0

    0

    1

    1

    1

    1

    1

    ?

    ?

    1

    ?

    ?

    1

    1

    0

    1

    1

    1

    ?

    18B Infratectum

    ?

    0

    1

    2

    1

    1

    1

    1

    1

    ?

    ?

    1

    ?

    ?

    1

    1

    1

    1

    1

    1

    ?

    19B Exine

    1

    0

    1

    0

    1

    1

    1

    1

    1

    ?

    ?

    1

    ?

    ?

    1

    1

    1

    1

    1

    1

    ?

    20B MicroGpts

    ?

    2

    1

    1

    0

    0

    ?

    2

    1

    ?

    1

    2

    2

    2

    2

    ?

    ?

    ?

    ?

    ?

    1

    21B MegaSphylls

    2

    2

    1

    1

    0

    0

    ?

    2

    1

    ?

    1

    2

    2

    2

    2

    ?

    1

    ?

    ?

    ?

    1

    22B Ovule to Sphyll

    ?

    0

    1

    1

    1

    1

    1

    0

    1

    0

    ?

    1

    ?

    0

    0

    1

    0

    0

    1

    1

    1

    23B Ovule Position

    ?

    1

    0

    0

    0

    0

    0

    1

    1

    0

    ?

    1

    ?

    1

    1

    0

    0

    0

    0

    0

    0

    24B Integm/Testae

    1

    1

    1

    1

    0

    0

    1

    1

    1

    ?

    1

    1

    1

    1

    1

    ?

    1

    ?

    1

    0

    1

    25B Megasgm/Nuc

    ?

    1

    0

    0

    0

    0

    ?

    1

    0

    ?

    0

    0

    1

    1

    1

    ?

    0

    ?

    ?

    ?

    0

    26B MegaGpts

    ?

    1

    0

    0

    0

    0

    ?

    1

    0

    ?

    0

    0

    1

    1

    1

    ?

    0

    ?

    ?

    ?

    0

    27B Sperm Transfer

    ?

    1

    1

    1

    ?

    0

    ?

    1

    1

    ?

    0

    1

    1

    1

    1

    ?

    ?

    ?

    ?

    ?

    1

    28B Fertilization

    ?

    1

    0

    0

    0

    0

    ?

    1

    0

    ?

    0

    1

    1

    1

    1

    ?

    ?

    ?

    ?

    ?

    ?


    Student problems. First, how could we combine the Process ANTHO and Process PTDSP sample analyses presented above while at the same time including additional characters?

    Second, can we tighten the selection of semaphoronts for study by selecting a species, rather than a genus, family, or order?

    Third, is it possible to develop genomic and/or molecular data sets to generate calibrated tool kit phylogenies and tests that support the notion of an evo-devo Process ANTHO and Process PTDSP?

    Fourth, how could Professor Crepet's early attempt to minimum age map basal flowering plants (2004) be updated to include the 123-124 million year old eudicot Leefructus (G. Sun et al. 2011)?

    Additional student problems, among others, include:

  • Expand the list of characters to include findings of the recent review on the evolution of seeds by Linkies et al. (2010) and evo-devo of secondary growth (Rachel Spicer and A. Groover 2010)
  • Practice using TREEVIEW (R. D. M. Page 1996) or other freeware to display phylograms resulting from application of PAUP algorithms to the data matrixes in Tables 4-5
  • Design a molecular phylogenetic analysis of molecular tool kits to analyze hypothetical evo-devo processes ANTHO, PTDSP, lycopsid, among others, by applying genomic data
  • Root the tool kit phylogenetic analysis and calibrate with fossils in a temporal context
  • Now carry out a combined morphological and tool kit phylogenetic analysis
  • Focus the morphological phylogenetic analysis on one or more of the deeply divergent paraphyletic clades of Paleozoic gymnosperms and recompute to identify heterochronic lineages (chronoclines)
  • Conduct a finer analysis of anatomical characters e.g. xylary conducting elements to detect and test for heterochrony using Hufford's methods (2002) to include new data on Gnetales (Carlquist 1996), heterochronous evo-devo of conducting tissues expressed in certain basal angiosperms (Carlquist 2009), and aspects of cell wall lignin polymer biosynthesis specifically presence or absence of angiosperm-specific syringyl (S) subunits (Zhao et al. 2010).
  • Perform morphological phylogenetic tests of these 300 million-year-old angiosperm-gymnosperm divergences to identify heterochronies
  • Design a cladistic study comparing tool kit and morphological phylogenetic analyses with published relaxed clock studies (Magallón 2010, Stephen A. Smith et al. 2010)
  • Figure a means to account for at least one intergeneric natural hybridization event in at least one of the morphological phylogenetic analyses e.g. between Delnortea abbottiae and Vojnovskya paradoxa
  • Based on the results of the preceding analyses are flowering plants (or, alternatively seed plants as a whole) monophyletic or paraphyletic?

    How many paraphyletic lines of gymnosperms, if any, are discernable from these analyses?

    Are past ideas of a late Jurassic or early Cretaceous monophyletic origin of angiosperms supported by your analyses?

    Problems for advanced students of paleobotany and phylogenetics. Many questions in evolutionary ecology may be answered, in part, by applying sophisticated cladistic and computational methods. Some questions, among others, might include:

    How can the phylogenetic analyses in the bulleted list above be refined to account for differential rates of divergence in the clades you have resolved using methods published by Quental and Marshall (2010), among others?

    Could you devise methods for comparing cladogenesis of coevolving insect antagonist and seed plant host lineages?

    Do these phylogenetic methods fit with studies published by population ecologists on escape and radiation and/or oscillation, and pollinator shifts?

    What do your analyses add to conclusions by Jiao et al. (2011) on the timing of swarms of WGDs as related to the Great Late Paleozoic Seed Plant Divergences and origin of flowering plants from the MRCA?

    One paleobotanist advocates combined molecular- and morphological-phylogenetic analyses to better understand evolution of flowers (J. A. Doyle 2001, 2008). Yet, from an evo-devo research perspective homologies of certain seed plant reproductive organs are problematic (see previous sections). Questions posed in this last student problem may be relevant.

    In the previous chapter we learned that the fossils pictured on either side of this page are the foliar remains of Lower Permian gymnosperms. Further, these two leaf forms almost always occur together in similar bedding planes of more than 12 surface exposures on two different continents, and in core samples pulled-up from bore-holes (three exploratory wells).

    Do these detached leaves belong to the same seed plant or two different, but sympatric species? The two slabs imaged were found at one surface locality in southwestern North America. The permineralized material from this bed is limonite. By studying these two slabs (same scale) what can be learned about the depositional environment of the bed including taphonomic factors such as energetics of burial?

    There are studies in the paleobotanical and physiological literature on the evolutionary-development (evo-devo) of auxin regulation. Further, auxin-based polarity networks (PINs) are deeply conserved. Based on a leaf-margin and midrib analysis of the two specimens pictured, and by knowing the vascular anatomy of the midrib of Delnortea abbottiae (Mamay et al. 1988), is there paleobiological evidence of auxin regulation of transcription factors (TFs) genetically expressed as these opposing morphologies?

    Using constructs based on theoretical morphospace published by contemporary paleobiologists, Professors Knoll, McGhee, and Niklas, reconstruct the most likely morphologies of the shoots that produced the foliage preserved in these two slabs. Were the shoot apical meristems (SAMs) found on the same mother plant or at the tips of branches on separate individuals?

    The final essay, which is located on another page covers the evolution, fossil history, paleobiodiversity, and radiation of Mesozoic flowering plants and basal angiosperms.


    Conclusions on the Paleobotany of Angiosperm Origins:

    Based upon a review of the literature and some of the ideas discussed in my essay on the origin of flowering plants, and the fragmentary paleobotanical evidence reported herein, I conclude that Paleozoic gigantopteroids and possibly Vojnovskyales are potential ancestors of the angiosperms.

    Baum and Hileman's (2006) hypothesis and related models of cone- and floral tool kit evolution reviewed by Melzer et al. (2011) are the most plausible ideas on the evo-devo of the flower.

    Evidence from molecular phylogenetics of several key homeotic selector genes, homeodomain proteins, and auxiliary TFs and miRNAs of their CRMs, which has come from increasingly elegant biomolecular studies of gymnosperm and flowering plant laboratory model organisms, points toward deep conservation in the regulatory machinery underpinning cone and floral morphological development (Theißen and Becker 2004, Floyd et al. 2006, Floyd and Bowman 2007, Nardmann et al. 2009, Specht and Bartlett 2009, Melzer et al. 2010, among others).

    My first essay placed an interesting idea on the table, namely that insect-seed plant interactions including horizontal transfer of mobile chromosome parasites, signaling, and thigmo, reinforced by temperature extremes and global hypoxia, might have led to coevolutionary development of cone and floral reproductive modules and moulting novelties of insect segments and appendages.

    The origin of angiosperms and certain clades of holometabolous insects is potentially a consequence of coevolution of animal and seed plant CRMs and developmental tool kits.

    Transposable elements are a potentially unstudied yet ostensibly critical ingredient in genome dynamics with potentially profound effects on transcription, translation, enzyme folding, and coevolution of manufactured homeodomain proteins. Amino acids including lysine residue 390 of the LFY-C primary polypeptide chain, and secondary HTH coiling of homeodomain proteins e.g. Tc3 transposase, Hin recombinase, insect Engraled, and LFY, are noteworthy clues (Hamès et al. 2008) and possible signatures suggesting cross-Kingdom TE activity.

    Further, I suggest that phytoecdysones secreted by Permo-Carboniferous and Permo-Triassic shrub lifeboats, which were essentially coevolutionary compartments, potentially affected body size and moulting time in phytophagous Holometabola.

    Douglas E. Soltis et al. (2007) suggest that WGDs were important in the early evolution of the angiosperm stem group.

    "It is noteworthy that polyploidy is absent in some ancient plant lineages, such as the cycads, which argues against the proposition that the frequency of polyploidy in a lineage is merely of symptom of lineage age (Fig. 9)."

    The preceding quotation is from page 376 of W. L. Crepet and K. J. Niklas, (2009), Darwin's second "abominable mystery": Why are there so many angiosperm species? American Journal of Botany 96(1): 366-381.

    Ancient WGDs are implicated in both the common ancestor of eudicots and monocots and in the MRCA roughly coinciding with the DeCARB and TrCCE. Further, an exhaustive genomic study of the cultivated grape overwhelmingly supports the existence of paleohexaploidy (Jaillon et al. 2007), which is equivalent to the "γ triplication" cited by Jiao et al. (2011).

    Logically, floral archetypes should be sought among fossilized whole plants and detached pieces (e.g. leaves, ovules, pollen) mined from rocks which are Carboniferous or Permian in age. This means that Mesozoic pteridosperms including cupule-forming Caytoniales were not ancestors of the flowering plants. Past proposals on a Cretaceous origin of angiosperms are absolutely incorrect.

    How might fossilized pieces or whole plants of Paleozoic ancestors of flowering plants appear to a paleobotanist, based upon knowledge gained from model systems of homeodomain proteins and FLO/LFY TFs of seed plant SAMs?


    A hypothetical 300 million year old gigantopteroid ancestor of the angiosperms might have been a woody shrub or vine supported by Aculeovinea yunguinensis- or Vasovinea tianii-type stems. The vegetative long shoots were possibly clothed by clasping Evolsonia texana-type gigantopteroid leaves representing a complete range of leaf shapes.

    Massive protoflowers may have developed from lateral spur shoots made-up of a bracteopetaloid perianth composed of a spiral of heteroblastic tepals, pigmented Lonesomia mexicana-type andropetals, spirally-arranged laminar microsporophylls (bearing pollen sacs), and an internal ring of Phasmatocycas bridwellii-type or Sobernheimia jonkeri-type ovule-bearing leaves.

    Fertile appendages and perianth parts might have grown from the apex of a fertile SAM or short (spur) shoot, representing reproductive organs of a completely new kind of gigantopteroid seed plant.

    Are the aforementioned proposals consistent with studies by Flores-Rentería et al. (2011) and Rudall et al. (2011) of recurrent abnormalities in conifer cones?

    The diagram shown above is a piece of a hypothetical plant with two protoflowers borne on spur (short) shoots, and a long shoot clothed with Evolsonia texana-like gigantopteroid leaves. Each spur shoot consisting of spirally arranged taeniopteroid bracts and sporophylls might have been subtended by a gigantopteroid leaf, such as the Evolsonia texana-like clasping appendage shown on the diagram.

    Paleozoic gigantopteroid proanthostrobili are not unlike Arber and Parkin's Mesozoic protoflowers or the model of the angiospermous strobilus (page 44, Figure 1, 1907).

    Based on supposed deep conservation in AP3 and the TFs they encode (Bharti Sharma et al. 2011), were some of the traits expressed in taeniopteroid tepals of gigantopteroid protoflowers (i.e. retuse apices and Clusia-like venation patterns) representative of early petals?

    A growing body of paleontologic evidence indicates that a wide range of detached gigantopteroid, taeniopterid, and vojnovskyalean leaf morphotypes existed during the Permian and Carboniferous Periods (T. N. Taylor et al. 2009). Many species of gigantopteroid seed plants might have existed during the late Carboniferous and throughout the Permian Period, offering ample opportunities for interspecific and intergeneric hybridization in sympatric populations.

    Hints on the morphology of hermaphroditic protoflowers of these gigantopteroid seed plants may be inferred from anatomical study of the bases and vascular traces of detached, fossilized leaves described from Carboniferous and Permian rocks.

    Fossiliferous Permo-Carboniferous sedimentary rock formations and associated continental cratons were pieced together by plate tectonics to form the Triassic Pangaean supercontinent. Isolated patches of terrestrial vegetation and fragmented biomes containing early angiosperms, conifers, and other lignophytes and monilophytes persisted in depauperate Triassic landscapes following the EPE.

    Except for certain Paleozoic Vojnovskyales the enigmatic Triassic seed plant Sanmiguelia lewisii and later Mesozoic bennettitaleans and pentoxylaleans, whole spur shoots and SAMs are rarely preserved in the fossil record or incompletely described.

    When supported by fossil calibrated phylogenetic tests of possible heterochrony in floral evo-devo of the unstudied chronocline linking Vojnovskya with Sanmiguelia, would the assertion quoted below be correct?

    "... major innovations in floral evolution do not coincide with the recovery stages following mass extinctions ..."

    The passage above is quoted from page 124 of J. C. McElwain, K. J. Willis, and K. J. Niklas (2011), 5. Long-term fluctuations in atmospheric CO2 concentration influence plant speciation rates. Pp. 122-140 In: T. R. Hodkinson, M. B. Jones, S. Waldren, and J. A. N. Parnell (eds.), Climate Change, Ecology and Systematics. Cambridge: Cambridge University Press, 524 pp.

    Over the many millions of years following the EPE, surviving populations of gigantopteroid shrub lifeboats with their resident insect antagonists probably coevolved leading to a potentially neotenous angiosperm ghost lineage, followed by the apparent explosive radiation of basal angiosperms, monocot, and eudicot flowering plants more than 100 million years later.

    The explosion of diversity of phytophagous coleopterans and dipterans following the EPE predates the oldest known flowering plants by more than 100 million years.

    Were shrub- and tree- dwelling Permo-Carboniferous Antliophora or Permo-Triassic beetles and flies responsible for angiospermization in several disparate and paleogeographically-remote lines of seed plant evolution?

    Conservation among plant MYB TFs (Rosinski and Atchley 1998) and insect olfactory, gustatory, and vision-related proteins (G. Zhang et al. 2007) inferred from studies of brain organization and mushroom bodies in model arthropods (Strausfeld 2009) leaves open the possibility that ancient seed plants of Paleozoic biomes might have attracted and/or repelled insects such as paleodictyopterans and panorpoids.

    Further, allometric scaling in paleoherbivore body size and the fertile plant organs they used for food, may suggest a potential evo-devo connection. Perhaps future allometric scaling studies of insect bodies and the host plant organs they inhabit or ingest for food may provide additional fuel to the idea of coevolution of insect and seed plant development tool kits and CRMs.

    Coevolution between insects and their host plant shrub lifeboats might have led to angiospermization in several groups of unrelated Carboniferous, Permian, and Triassic seed plant groups and the ongoing arms race. A complex and necessary coevolutionary interplay probably existed between resident phytophagous insects and their host seed plants, starting at the physiologic and genetic level, reinforced by global catastrophe, temperature extremes, and low pO2.

    Selection pressures in populations of Permo-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.

    Understanding selective pressures behind molecular coevolution of insect and seed plant developmental cis-acting TFs in deep-time i.e. hundreds of millions of years, might be an important first step in unraveling the enigmatic origin of angiosperms, evo-devo of the perianth and protoflowers, and adaptive radiation of certain clades of coevolving Holometabola.

    Scientific evidence is needed in several critical areas of inquiry, among others:

  • To describe the fitness landscape and model mutualism inside early Carboniferous, Permian, and Triassic shrub lifeboats
  • To model the aerodynamics of monopodial shrub lifeboats, potential oxygenation, and insulating properties of plant crevices and air spaces around sheathing leaves, compared to other seed plant growth forms indigenous to island archipelago frozen paleoenvironments of the DeCARB and in later continental warmer and drier Permian times and places
  • To identify from fossils, specific insect species indigenous to shrub- and tree-like lifeboats
  • To expand the study of TSBs including the stratigraphic distribution of the geomolecular tracer oleanane in fossilized leaves and reproductive structures of Carboniferous, Permian, and Triassic seed plants
  • To explain the nature and biomechanical details of phytophagous insect-plant associations inferred from anatomical study of permineralized material at early and late stages of development
  • To ascertain specific external biotic and environmental factors affecting evo-devo of larval moult cycles and innovative mouthpart designs of phytophagous insects
  • To determine which role, if any, cross-Kingdom transposon movements played in a Paleozoic origin of the holometabolous bees, beetles, flies, and wasps, and in the evo-devo of cones and protoflowers
  • To find and describe convincing protoflowers in Paleozoic rocks within intervals in geologic time predicted by molecular phylogenies of homeotic selector genes and TFs
  • To understand the homology and polarization of seed plant morphological characters as a prelude to rescoring and reanalyzing data sets
  • To fill-in the stratigraphic gaps in the seed plant fossil record by mining and studying more fossils
  • To calibrate seed plant tool kit phylogenies with fossils
  • To identify the 160 million year old angiosperm ghost lineage by training more paleontologists and funding their research
  • An early 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 CAMP, which is associated with the 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 (Hunt et al. 2007).

    When taking into account the cyclic nature of angiospermization, flowering plants as traditionally defined might be an amalgam of paraphyletic evolutionary lines traceable to surviving geographically disparate early Triassic remnants of already divergent Permian seed plant lineages.

    While discussing the presumed "obsession" by paleobotanists with study of extinct gymnosperms; and Stewart and Rothwell's (1993) observation that the four major lineages of extant non-angiospermous seed plants (cycads, Ginkgo, conifers, and Gnetales) constitute a small sampling of seed plant paleobiodiversity, Bateman et al. (pages 3488-3499, 2006) state:

    "It is therefore feasible, and even likely, that these groups plus the angiosperms arose as independent lineages from within the plexus of wholly extinct gymnosperms."

    The preceding statement is quoted from page 3489 of R. A. Bateman, J. Hilton, and P. J. Rudall (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.

    Further, Paleozoic seed plants such as gigantopteroids and hermaphroditic Vojnovskyales should be included in future phylogenetic analyses by paleobotanists now that biochemists infer the first appearance of homeotic B-gene regulation by protein quartets in the last common gymnosperm ancestor before the angiosperm-conifer split roughly 300 MYA (Theißen and Becker 2004).

    Molecular dating of the angiosperm divergence from the MRCA remains an important piece of the puzzle, which could allow paleobotanists to better focus their quest for the ancestor of angiosperms (or its detached pieces) in late Paleozoic rocks. Putative great late Paleozoic divergences have yet to be properly calibrated sensu Marshall (2008) with fossil evidence of 300 million year old gigantopteroid and vojnovskyalean protoflowers.

    Poorly known Paleozoic seed plants including gigantopteroids and vojnovskyaleans may be surprising contributors to the genomes of Triassic "angiosperms" (including Sanmiguelia and bennettitaleans). All five of the aforementioned seed plant groups (bennettitaleans, gigantopterids, gigantopteroids, Sanmiguelia, and vojnovskyaleans), should be included in phylogenetic analyses of seed plants.

    Ancestors of putative paraphyletic grades of angiosperms might have been gymnosperms with hermaphroditic strobili. I also built a case and presented evidence in the second essay that some of the candidate gymnosperm groups with bisexual protoflowers are presently known only from detached heteroblastic taeniopteroid sporophylls and foliar tepals of Ginkgo-like spur shoots subtended by gigantopteroid megaphylls.

    I conclude that insect-mediated intergeneric natural hybridization among populations of Paleozoic gigantopteroids and possibly Vojnovskyales, followed by spontaneous paleopolyploidy, might have been a method through which MIKC-type MADS-box gene duplicates were generated, later spreading molecular novelties in populations of the ancestral early Triassic ghost lineages of angiosperms that survived the EPE.

    Further, our knowledge of carpel, floral, and ovular transcriptional regulators in extant angiosperm model organisms does not preclude derivation of evo-devo models that explain curling, inrolling, and fusion in Permo-Carboniferous ovule-bearing spermopterid Phasmatocycas bridwellii leaves to form carpels, ovaries, and pistils.

    One hundred and sixty million years of seed plant neotenic evolution to include condensation of hypothetical gigantopteroid protoflowers could be most simple evo-devo process to explain the origin of reproductive organs in Mesozoic crown group angiosperms and extant basal Amborellanae, Austrobaileyanae, Nymphaeanae, and Magnolianae from late Paleozoic ancestors.

    When my proposals are supported by additional paleobotanical studies and future fossil calibrated tool kit phylogenetic analyses, a paraphyletic origin of angiosperms from the MRCA becomes likely. If true, then many published phylogenetic reconstructions of seed plant lineages leading to flowering plants and past ideas on the origin of angiosperms are incorrect.


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    ESSAY CONTENTS

  • Arthropod Assemblages: Paleoentomology of Palynivores and Pollinators
  • Asian Gigantopterids
  • Bennettitales
  • Caytoniales
  • Character Analysis and Homology Assessment
  • Conclusions on the Paleobotany of Angiosperm Origins
  • Corystospermales
  • Cycadales
  • Dating Angiosperm Divergences from the Most Recent Common Ancestor (MRCA)
  • Enigmatic Seed Plants of the Mesozoic
  • Evo-devo of Progymnosperm and Seed Plant SAMs: Paleozoic Splits
  • Floral Paedomorphism and Coevolving Body Allometries
  • Gigantopterids
  • Gigantopteroids or Gigantopterids? American Delnorteas and Evolsonias
  • Glossopteridales
  • Gnetales
  • Hypothetical Protoflowers of Gigantopteroids
  • Literature Cited on the Paleobotany of Angiosperm Origins
  • Mesozoic Evolution of Holometabolous Insects
  • Paleobotanical Challenges and Choices
  • Paleontologic Evidence
  • Paleozoic Origin of the Holometabola
  • Pentoxylales
  • Phasmatocycas and Other Spermopterids
  • Phylogenetic Considerations
  • Sanmiguelia
  • Seed Plant/Progymnosperm Phylogenetic Analyses
  • Seed Plants of the Mesozoic Era
  • Student Problems
  • Taxon-specific Biomarkers (TSBs)
  • Telombs, Trusses, and Potentially Tantalizing Questions
  • Tool Kits and Homology
  • Top-down and Bottom-up Approaches
  • Vojnovskyales

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    NOVEMBER 11, 2011


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