Paleobotany of Angiosperm Origins:
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E S S A Y C O N T E N T S
[ Paleobotany of Angiosperm Origins ]
JOHN M. MILLER, Ph.D.
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 holometabolus 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 gigantopterid 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), 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 gne-pine 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--
'via Blog this'
You are here: Paleobotany of Angiosperm Origins
E S S A Y C O N T E N T S
[ Paleobotany of Angiosperm Origins ]
JOHN M. MILLER, Ph.D.
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 holometabolus 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 gigantopterid 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), 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 gne-pine 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--
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