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

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Gigantopteroid news and commentary is complete with illustrations and links to scientific research articles, and discussion topics for debating the origin of angiosperms in classrooms, on the Internet, and in the halls of paleobiology.

An exposure of the Triassic Chinle Formation of southwestern North America is pictured to the left. Scott Williams, Petrified Forest National Park Curator and Photographer, captured colorful digital images of massive permineralized logs, which have been described as the morphospecies Araucarioxylon arizonicum, seed plant incertae cedis. Logs were weathered from Norian sedimentary beds deposited 220- to 225- million years ago (MYA).

The image on the right is a flowering branch of Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnolianae), which is indigenous to Viti Levu Island, Fiji. The image was captured by Professor Hervé Sauquet, Laboratoire Ecologie Systématique et Evolution, Equipe Evolution des Angiospermes, Université Paris-Sud, France, and is posted here with his written permission. Degeneriaceae figure prominently in classical ideas on the origin of flowering plants. Yet, the basalmost position of the Amborella (Amborellaceae) + Nuphar (Nymphaeaceae) couplet in APG III has no bearing on the ancestry or origin(s) of angiosperms, which remains as controversial and enigmatic as ever, despite advances in genomics, with little consensus on age estimates and geologic timing of cladogenesis and divergence from other seed plant groups.

Cupules and Ovules Inside a Permineralized Compound Cone from North American Valanginian Rocks (May 2016):

The American Journal of Botany publishes yet another significant paleobotanical study and morphological-phylogenetic analysis of seed plants by Gar Rothwell Ph.D. and Ruth Stockey, Ph.D. A permineralized compound cone recovered from a concretion found in a North American Valanginian rock outcrop on Vancouver Island yielded a surprising trove of cupules, ovules, axillary shoots, bracts, and megasporophylls attached to a mostly complete female cone axis.

Rothwell, G. W. and R. A. Stockey. 2016. Phylogenetic diversification of early Cretaceous seed plants: the compound seed cone of Doylea tetrahedrasperma. American Journal of Botany 103: 923-937.

This critically important research paper contains profound implications on deciphering the evolution of cones, cupules, flowers, ovules, pollination mutualisms, and the origin of flowering plants from [still] unknown seed plant ancestors in deep-time. Based on mounting evolutionary-developmental, morphological, and paleobotanical evidence, the floral bauplan is probably considerably more ancient than generally thought by Andre Chanderbali, P. R. Crane, J. A. Doyle, E. M. Friis, K. R. Pedersen, D. E. Soltis, and P. S. Soltis.

"FIGURES 10-15 Doylea tetrahedrasperma Stockey and Rothwell. All sections are from concretion P13467. (10) Longitudinal view of bract/axillary fertile shoot complex sectioned in approximately radial view of cone, showing diverging bract tip [b] and one sporophyll-bearing ovule. Note elongated scale tip [st], and recurved lobe of sporophyll [arrow] extending back along ovule side. Numbered lines at base of photo correspond to levels at which figures of same number are sectioned. C top no. 60, ×20 ..." This copyrighted figure was reproduced with written permission from the Editorial Office of the American Journal of Botany.

Based on this extraordinary fossil find, a new order of seed plants, Doyleales, was proposed by Rothwell and Stockey (2016). The presumed corystosperm species, Umkomasia mongolica, described by Gongle Shi et al. earlier in 2016, was transferred to Doylea by Rothwell and Stockey.

"Both Doylea species appear to have the same novel mode of development interpreted above. Of particular importance, Doylea is the only cupulate 'seed fern' to have the seeds borne in a compound seed cone of compact structure."

The preceding passage was quoted from the "DISCUSSION, Systematics, evolution, and spermatophyte diversification" on page 933 of Rothwell and Stockey (2016).

"Although the ovulate stalks of Ginkgo biloba occur on short shoots of indeterminate growth [rather than in a compound cone; Christianson and Jernstedt, 2009], they are not attached to the subtending leaf or bract, and the seeds are not inverted" (pages 934-935, Rothwell and Stockey 2016).

Importance of Mesozoic Caytoniales and Corystospermales in deciphering the anatomy and morphology of flowers, carpels, anatropous ovules, and double integuments (J. A. Doyle 2006, 2008, Shi et al. 2016) is fading. Based on a new morphological-phylogenetic analysis of spermatophytes by Rothwell and Stockey (2016), these two orders of seed plants and their Paleozoic glossopterid antecedents, probably had nothing to do with the origin of flowering plants.

"Different [contrasting] interpretations of the homology of corystosperm cupules have significantly different implications for understanding seed plant phylogeny, including the origin of angiosperms" (quoted from the Introduction on page 1419 of Shi et al. 2016).

Casting aside arguments in a classical 1978 paper by J. A. Doyle, which are refreshed in detailed discussion of pteridosperm and floral chronoclines (J. A. Doyle 1994), and YABBY TFs in seed plants (J. A. Doyle 2006), why is an understanding of the origin and paleobiology of the angiosperm second integument so critical in deciphering seed plant organ homologies in deep-time?

Biochemical and morphological evidence suggests that cones and flowers are reproductive short shoots. If fertile spur shoots are known from late Paleozoic fossils, and the floral SAM is a deeply conserved organ (Theißen and Melzer 2007, Becker 2016, among others), then how could the flower possibly originate in the late Mesozoic? Andre S. Chanderbali et al. (2016) seemingly resuscitate this paradox in the first sentence of their review. Genomic- and tool kit phylogenies and cladograms such as APG IV, unless calibrated with definitive fossils from accurately-dated stratigraphic horizons, are probably unhelpful in deciphering the origin of canalized cone and floral morphologies, and their deeply-conserved gene regulatory program including CRMs, GRNs, and PINs.

"While the amazing conservation of the major floral identity [ABCDE] program is being unravelled by analysing floral homeotic gene function and expression, we are only just beginning to understand the evolution of the gene network governing the organ identity genes ... " (Abstract Scope and Conclusions, page 145, Becker 2016, item in [brackets] is mine).

Calibration of phylogenies of cone and floral tool kit homeodomain proteins and TFs with fossils is necessary to bracket the interval in geologic time when flowers evolved. In view of the novel "fingerprint of developmental regulation" (quoted from page 723, Sanders et al. 2007) seen in the doylealean cone, it is may be prudent for Chanderbali and co-workers to define the seed plant cone and flower with morphological precision, and to rethink their ideas on evolution of Amborellanae and the timing of the appearance in the fossil record of the so-called first flower.

Gene expression studies of ovule determinants in extant flowering plants indicate that integumentary layers develop by simple splitting or fusion (Kelley et al. 2009; R. H. Brown et al. 2010). Simply put, there is no justification to omit discussion of ovule evo-devo when Gongle Shi and coworkers discuss the anatomy of the angiosperm second integument (page 1427, 2016).

Further, it is no surprise that gigantopteroids and Vojnovskyales were left-out of the discussion of seed plant phylogenies on pages 934-935 of Rothwell and Stockey (2016). These seed plant groups are "Gymnosperms with Obscure Affinities" (Chapter 19 on page 757 of T. N. Taylor et al. 2009).

Did species of certain Paleozoic seed plants with reproductive short- [spur-] shoots display an ancestral, developmentally-plastic, floral bauplan? Based on Figure 10 (see the left-hand image, above), species of Mesozoic Doyleales did not.

Taking into account the discussion above, and other aspects of seed plant evolution and character homologies developed elsewhere in this web site, paleobotanists should employ novel approaches such as discerning "fingerprints of developmental regulation" from tool kit studies to uncover and describe Permo-carboniferous seed plant groups as candidate ancestors of stem-group flowering plant lineages.

Paleobiologists should not forget that intergeneric hybridization and allopolyploidy, facilitated by insect and/or wind cross-pollination of cones and protoflowers, might have been important in the population paleoecologies of these seed plants, including [paraphyletic] stem group[s of] angiosperms. Diploidization of polyploids should be considered by Chanderbali et al. (2016) when interpreting the fate of genomes in hybridizing seed plant populations at the heart of the alpha- [α-] swarm of whole genome duplications (WGDs) preceding or contributing to late Paleozoic seed plant divergences.

Further Reading:

Becker, A. 2016. Tinkering with transcription factor networks for developmental robustness in Ranunculales flowers. Annals of Botany 117: 845-858.

Bomfleur, B., E. L. Taylor, T. N. Taylor, R. Serbet, M. Krings, and H. Kerp. 2011. Systematics and paleoecology of a new peltaspermalean seed fern from the Triassic polar vegetation of Gondwana. International Journal of Plant Sciences 172(6): 807-835.

Brown, R. H., D. L. Nickrent, and C. S. Gasser. 2010. Expression of ovule and integument-associated genes in reduced ovules of Santalales. Evolution and Development 12: 231-240.

Chanderbali, A. S., B. A. Berger, D. A. Howarth, P. S. Soltis, and D. E. Soltis. 2016. Evolving ideas on the origin and evolution of flowers: new perspectives in the genomic era. Genetics 202: 1255-1265.

Christianson, M. L. and J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: a quantitative analysis of the disposition of axillary structures. American Journal of Botany 96(11): 1957-1966.

Doyle, J. A. 1978. Origin of Angiosperms. Annual Review of Ecology and Systematics 9: 365-392.

Doyle, J. A. 1994. Origin of the angiosperm flower: a phylogenetic perspective. Plants Systematics and Evolution (Supplement) 8: 7-29.

Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. The Journal of the Torrey Botanical Society 133(1): 169-209.

Doyle, J. A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169(7): 816-843.

Kelley, D. R., D. J. Skinner, and C. S. Gasser. 2009. Roles of polarity determinants in ovule development. The Plant Journal 57: 1054-1064.

Rothwell, G. W. 1987. The role of development in plant phylogeny: a paleobotanical perspective. Review of Palaeobotany and Palynology 50: 97-114.

Sanders, H., G. W. Rothwell, and S. E. Wyatt. 2007. Paleontological context for the developmental mechanisms of evolution. International Journal of Plant Sciences 168: 719-728.

Shi, G., A. B. Leslie, P. S. Herendeen, F. Herrera, N. Inchinnerov, M. Takahashi, P. Knopf, and P. R. Crane. 2016. Early Cretaceous Umkomasia from Mongolia: implication for homology of corystosperm cupules. New Phytologist 210: 1418-1429.

Stockey, R. A. and G. W. Rothwell. 2009. Distinguishing angiophytes from the earliest angiosperms: a Lower Cretaceous (Valanginian-Hauterivian) fruit-like reproductive structure. American Journal of Botany 96(1): 323-335.

Taylor, E. L. and T. N. Taylor. 2009. Seed ferns from the late Paleozoic and Mesozoic: any angiosperm ancestors lurking there? American Journal of Botany 96(1): 237-251.

Taylor, E. L., T. N. Taylor, H. Kerp, and E. J. Hermsen. 2006. Mesozoic seed ferns: old paradigms, new discoveries. Journal of the Torrey Botanical Society 133(1): 62-82.

Taylor, T. N., E. L. Taylor, and M. Krings. 2009. Paleobotany: The Biology and Evolution of Fossil Plants, Second Edition. Burlington: Elsevier Academic Press, 1230 pages.

Theißen, G. and R. Melzer. 2007. Molecular mechanisms underlying origin and diversification of the angiosperm flower. Annals of Botany 100(3): 1-17.



Convergence in Kalligrammatids and Papilionoids, and Angiosperm Mutualisms with Holometabola (February 2016):

The Royal Society publishes yet another significant study detailing some aspects of the development of pollination mutualisms between holometabolous insects and seed plants, arthropod antagonism, possible coevolution, and trait convergence. Kalligrammatids having preserved wing eyespot scales are reported from the Middle Jurassic Jiulongshan Formation, and in younger beds of the Karabastau and Yixian Formations of central and eastern Asia.

Labandeira, C. C., Q. Yang, J. A. Santiago-Blay, C. L. Hotton, A. Monteiro, Y-J. Wang, Y. Goreva, C-K. Shih, S. Siljeström, T. R. Rose, D. L. Dilcher, and D. Ren. 2016. The evolutionary convergence of mid-Mesozoic lacewings and Cenozoic butterflies. Proceedings of the Royal Society of London, Series B, Biological Sciences 283(1824): 20152893.

The right-hand image is a papilionoid butterfly visiting a flowering head of Achillea millefolium (Asteraceae, Asterales, Asteranae). The eyespots and melanized scales of the insect wings are visual cues for predators.

Convergent traits of the lepidopterans and neuropterans discussed by Labandeira et al. (2016) include chemical and structural aspects of wing eyespots and scales and mouthpart morphologies.

"Our data also suggest that if angiosperms antedated the mid-Early Cretaceous and were insect pollinated, they most likely harboured associations with mandibulate rather than long-proboscid insects, consistent with early angiosperm floral structure ..." (quoted from 4. Discussion and Conclusion, Labandeira et al. 2016)

"Which came first: the butterfly or the flower?"

The preceding quote is from the title of a news story published by The Guardian highlighting the study by the Labandeira team.

In my opinion, seed plant species with flowers are considerably older than Lepidoptera and Thysanoptera. Flowers and protoflowers are probably as ancient as certain lineages of Coleoptera, Diptera, and Hymenoptera (the "big five" palynivores and pollinators, page 241, Labandeira 2000). Examples include Mesozoic bennettitalean protoflowers and flower-like organs (also protoflowers) of Late Paleozoic seed plants including Vojnovskyales and other species assignable to several orders of gymnosperms that bear reproductive short- [spur-] shoots.

Supplementary Reading:

Briscoe, A. D. and L. Chittka. 2001. The evolution of color vision in insects. Annual Review of Entomology 46: 471–510.

Chittka, L. 1996. Does bee color vision predate the evolution of flower color? Naturwissenschaften 83: 136-138.

Chittka, L., J. Spaethe, A. Schmidt, and A. Hickelsberger. 2001. 6. Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision. Pp. 106-126 In: L. Chittka and J. D. Thomson (eds.), Cognitive Ecology of Pollination, Animal Behaviour and Floral Evolution. Cambridge: Cambridge University Press, 344 pp.

Janz, N. 2011. Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Annual Review of Ecology, Evolution, and Systematics 42: 71-89.

Labandeira, C. C. 1998. How old is the flower and the fly? Science 280: 57-59.

Labandeira, C. C. 2000. The paleobiology of pollination and its precursors. Pp. 233-269 In: R. A. Gastaldo and W. A. DiMichele (eds.), Phanerozoic Terrestrial Ecosystems. Paleontological Society Papers 6: 233-269.

Ren, D. 1998. Flower-associated Brachycera flies as fossil evidence for Jurassic angiosperm origins. Science 280: 85-88.

Ren, D., C. C. Labandeira, J. A. Santiago-Blay, A. Rasnitsyn, C-K. Shih, A. Bashkuev, M. A. V. Logan, C. L. Hotton, and D. L. Dilcher. 2009. A probable pollination mode before angiosperms: Eurasian, long-proboscid scorpionflies. Science 326(5954): 840-847.



A New Family of Evolutionarily Advanced "Unsolved" Ceratophyllales from the Barremian 125 MYA (October 2015):

Use of the word "unsolved" in header for this news commentary may be traced to the title of a significant publication in the American Journal of Botany by Akitoshi Iwamoto et al. (2015) detailing some aspects pertaining to phylogenetics and morphologies of extant Ceratophyllum demersum (Ceratophyllaceae, Ceratophyllales, Magnoliidae [flowering plant incertae cedis]).

Iwamoto, Akitoshi, Ryoku Izumidate, and L. P. Ronse De Craene. 2015. Floral anatomy and vegetative development of Ceratophyllum demersum: a morphological picture of an "unsolved" plant. American Journal of Botany 102(10): 1578-1589.

This is Figure 1 from Akitoshi Iwamoto et al. (2015), which is reproduced by written permission of Professor Iwamoto of Tokyo Gakugei University and Kodan-sha [4-1-1 Nukui Kita-machi, Koganei-shi, Tokyo 184-8501, JAPAN]. I thank the American Journal of Botany Editorial Office for coordinating the necessary written permissions from the publisher in Japan.

The Iwamoto team discusses vegetative phyllotaxis of this plant and scanning electron microscopy of developing staminate and pistillate flowers offers a window on floral development in Ceratophyllum demersum (Akitoshi Iwamoto et al. 2003).

Are the lateral shoot apical meristems (SAMs) and flowers of Ceratophyllum demersum depicted in Figures 2-8 (Akitoshi Iwamoto et al. 2015), homologous with vegetative and reproductive short-shoots of Ginkgo biloba?

"FIGURE 1 Ceratophyllum demersum L. (A) Shoot in aquatic environment. (B) Vegetative buds covered with prophylls, in the axil of a leaf. (C) Staminate flower consisting of numerous stamens and surrounding bracts. (D) Pistillate flower consisting of only one pistil with long stigma and surrounding bracts. b, bract; l, leaf; p, prophylls; st, stamen; sti, stigma. Scale bars = 1 cm (A); 500µm (B-D). Photographs are from Akitoshi Iwamoto (2012) with permission," copyright ©2012 Kodan-sha, Tokyo, Japan.

Paleobiology of ceratophyllaleans. The Iwamoto team's study appeared about one month following further discussion of ancient Montsechia vidalii (Montsechiaceae, Ceratophyllales), which was published in the Proceedings of the National Academy of Sciences by Bernard Gomez et al. (2015).

"Based on its unparalleled morphological features, D. H. Les (1988) suggested that the genus [Ceratophyllum] is [was] closest to ancestral angiosperms" (Introduction on page 1578, Akitoshi Iwamoto et al. 2015, the words in [brackets] are mine).

With respect to the Bernard Gomez et al. 2015 paleontological study, which is also a focus of this news clip (see the header, above), Montsechia vidalii has been known to paleobotanists for several decades as an aquatic liverwort assigned to Jungermanniales. Affinities of Montsechia with angiosperms was suggested later (Martín-Closas 2003).

"... Ceratophyllaceae are truly 'living fossils' and represent plants which probably diverged from some of the earliest angiosperm progenitors ..." (Conclusions on page 341, D. H. Les 1988).

These authors propose the family Montsechiaceae, placed as sister to flowering plants within the context of APG III.

"... the fossil angiosperm presented here [Montsechia], raises questions centered on the very early evolutionary history of angiosperms. The importance of very early aquatic flowering plants, perhaps basal to all angiosperms [they are not, in my opinion], as previously proposed [G. Sun et al. 1998], merits serious consideration and reevaluation" (page 10987, Bernard Gomez et al. 2015, comments in [brackets] are mine).

Gomez, B., V. Daviero-Gomez, C. Coiffard, C. Martín-Closas, and D. L. Dilcher. 2015. Montsechia, an ancient aquatic angiosperm. Proceedings of the National Academy of Sciences 112(35): 10985-10988.

What "merits serious consideration and reevaluation," in my opinion, is a high probability that several populations of basal flowering plants and magnoliids, monocots, and eudicots, including ceratophyllaleans, coexisted in multiple aquatic and terrestrial environments in Jurassic times and places, and that New Caledonian populations of Amborella trichopoda had little or nothing to do with the origin of flowering plants. This view contrasts with discussion by J. A. Doyle (2012) on the molecular-phylogenetic placement of Ceratophyllum in relation to ANA-grade basal angiosperms, Chloranthaceae, and eudicots.

Homology of ceratophyllalean organs with characters of extinct seed plants. Several morphological structures seen in extant species of Ceratophyllum are probably homologous with features of the anatomy and morphology of certain living cycads and conifers, and Upper Paleozoic Callistophytales and Vojnovskyales. Specific examples are wind-dispersed pollen described as the Pennsylvanian callistophytalean morphogenus Vesicaspora (Figure 14.170 on page 598 of T. N. Taylor et al. 2009) and haustorial pollen tubes of certain extant species of Cycadales (D. H. Les 1988).

Morphologies of Ceratophyllum leaves bear some resemblance to fan-shaped sporophylls of Sandrewia texana (Figure 15.72 and 15.73 on pages 647 and 648, T. N. Taylor et al. 2009), which is a Late Paleozoic genus of probable Vojnovskyales (Mamay 1975). No one to date has suggested homologies of organs of Ceratophyllales with extinct Vojnovskyales. This idea should be explored, in my opinion.

Further, branched pollen tubes are observed in Ceratophyllum (D. H. Les 1988, 1993). The startling but often overlooked observation opens the floor to four questions, among others:

Is the developmental program of pollen-containing microgametophytes and reproductive short shoots of Ceratophyllum identical to certain gymnosperm species?

Could Ceratophyllum demersum, Ceratophyllum echinatum, or Ceratophyllum submersum become new model species for gene expression and genomic studies, or new lines of research on DNA-binding (homeodomain) transcription factors (TFs)?

Are aquatic and herbaceous Ceratophyllales better nested with an extinct (or extant) group of gymnosperms than with basal angiosperms (amborellas and water lilies) or magnoliids and eudicots?

When supported by biochemical, genetic, and morphological data, are flowering plants in the broad sense, including Ceratophyllales and monocots, comprised of several paraphyletic lineages once capable of intergeneric hybridization in long-extinct sympatric populations?

Concluding remarks. While challenging a so-called Amborella + Nymphaea "paradigm" (Amborellanae and Nymphaeanae are not linchpins of angiosperm history but reflect non-paradigmatic tree-thinking), the paper by Bernard Gomez et al. (2015) bypasses Cornet (1989), Cornet and Habib (1992), Hochuli and Feist-Burkhardt (2004, 2013), and Xin Wang (see below) findings, leaving out possibly critical points for debating the paleoecologies of stem group flowering plants.

Paleobotanical evidence published by Cornet, Hochuli and Feist-Burkhardt, and Xin Wang and coworkers calls into question a whole body of paleophysiologic work on the ecologies of so-called "early" angiosperms. In fact, palynological data gleaned from studies of several core samples recovered from more than one exploratory bore-hole posits more than three angiosperm populations indigenous to arid, boreal, and tropical environments, respectively, of Middle Triassic Pangaea (Hochuli and Feist-Burkhardt 2004, 2013). Paleoecologies of these ancient angiosperm populations were not "xerophobic," "dark and disturbed," or "wet and wild," or explainable by unproven paleophysiologic phenomena or pairing of nonsensical adjectives.

Did the earliest flowering plants evolve in aquatic environments as proposed by Dilcher, Martín-Closas, Sun Ge, and others? No, if Hochuli and Feist-Burkhardt palynological data are considered.

"... Are the angiosperms of an aquatic ancestry? Although evidence is mounting that implicates aquatic plants as descendants of early flowering plants, it is highly unlikely that the group evolved from aquatic ancestors ..." (Conclusions on page 10123, D. H. Les et al. 1991).

Interestingly, a chromosome base number of x = 12 has been reported for Ceratophyllaceae (D. H. Les 1988).

In conclusion, I already stated elsewhere on this web site that studies of the genomic landscape of Amborella trichopoda are probably unhelpful in discerning angiosperm stem groups of Permo-triassic times and places, proving intergeneric hybridization in ancient zones of sympatry, and elucidating reproductive mechanisms leading to allopolyploid formation and dispersal of hybrid offspring.

Would genomic studies of Ceratophyllum demersum help us understand evolutionary relationships of the species with Amborella trichopoda?

Are Ceratophyllales the aquatic descendants of woody Vojnovskyales with no evolutionary ties to crown group basal flowering plants and magnoliids, or eudicots or monocots?

Finally, two important papers, (1) a "Coastal Hypothesis" for the dispersal and radiation of ancient angiosperms (Retallack and Dilcher 1981) and (2), a report of fossilized Ceratophyllum from the Paleogene by Herendeen et al. (1990), among others, were not cited in this latest installment of Professor Emeritus Dilcher's long and distinguished publication record on fossilized flowers, and their paleobotany, taphonomy, and paleoecology.

In my opinion, these authors could adapt a well-reasoned "Coastal Hypothesis" to extend more deeply in geologic time to Artinskian and Cisuralian coastlines, and to the two "unsolved" gymnosperm species, Delnortea abbottiae and Evolsonia texana, as widespread gigantopteroid seed plant populations that potentially hybridized with certain species of Vojnovskyales, e.g. Sandrewia texana, spread across a couple thousand kilometers of tropical maritime swamps, riparian scrub and woodlands, and semiarid hills bordering the Hovey Channel of the Panthalassa Sea at the western end of the Central Pangaean Mountains.

Further Reading:

Cornet, B. 1989. Late Triassic angiosperm-like pollen from the Richmond Rift Basin of Virginia. Palaeontographica B 213: 37-87.

Cornet, B. and D. Habib. 1992. Angiosperm-like pollen from the ammonite-dated Oxfordian (Upper Jurassic) of France. Review of Palaeobotany and Palynology 71: 269-294.

Doyle, J. A. 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40: 301–326.

Gomez, B., V. Daviero-Gomez, C. Coiffard, C. Martín-Closas, and D. L. Dilcher. 2015. Montsechia, an ancient aquatic angiosperm. Proceedings of the National Academy of Sciences 112(35): 10985-10988.

Herendeen, P. S., D. H. Les, and D. L. Dilcher. 1990. Fossil Ceratophyllum (Ceratophyllaceae) from the Tertiary of North America. American Journal of Botany 77(1): 7-16.

Hochuli, P. A. and S. Feist-Burkhardt. 2004. A boreal early cradle of angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). Journal of Micropalaeontology 23: 97-104.

Hochuli, P. A. and S. Feist-Burkhardt. 2013. Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (Northern Switzerland). Frontiers in Plant Science, Plant Evolution and Development 4: Article 344.

Iwamoto, A. 2012. Ceratophyllum, Pp. 52-59 In: H. Tobe and M. Tamura (eds.), New Plant Systematics. Tokyo: Kodan-sha.

Iwamoto, A., R. Izumidate, and L. P. Ronse De Craene. 2015. Floral anatomy and vegetative development of Ceratophyllum demersum: a morphological picture of an "unsolved" plant. American Journal of Botany 102(10): 1578-1589.

Iwamoto, A., A. Shimizu, and H. Ohba. 2003. Floral development and phyllotactic variation in Ceratophyllum demersum (Ceratophyllaceae). American Journal of Botany 90(8): 1124-1130.

Les, D. H. 1988. The origin and affinities of the Ceratophyllaceae. Taxon 37(2): 326-345.

Les, D. H. 1993. Ceratophyllaceae. Pp. 246-250 In: K. Kubitzki, J. G. Rohwer, and V. Bittrich (eds.), The Families and Genera of Vascular Plants, Volume II, Flowering Plants - Dicotyledons, Magnoliids, Hamamelids, and Caryophyllids. Berlin, Springer.

Les, D. H., D. K. Garvin, and C. M. Wimpee. 1991. Molecular evolutionary history of ancient aquatic angiosperms. Proceedings of the National Academy of Sciences 88: 10119-10123.

Mamay, S. H. 1975. Sandrewia, n. gen., a problematical plant from the Lower Permian of Texas and Kansas. Review of Palaeobotany and Palynology 20: 75-83.

Martín-Closas, C. 2003. The fossil record and evolution of freshwater plants: a review. Geologica Acta 1(4): 315-338.

Retallack, G. J. and D. L. Dilcher. 1981. A coastal hypothesis for the dispersal and rise to dominance of flowering plants. Pp. 27-77 In: K. J. Niklas (ed.) Paleobotany, Paleoecology, and Evolution. New York: Praeger.

Sun, G., D. L. Dilcher, S.-L. Zheng, and Z. Zhou. 1998. In search of the first flower: a Jurassic Angiosperm, Archaefructus, from northeast China. Science 282(5394): 1692-1695.

Taylor, T. N., E. L. Taylor, and M. Krings. 2009. Paleobotany: The Biology and Evolution of Fossil Plants, Second Edition. Burlington: Elsevier Academic Press, 1230 pages.

The preceding diagram is redrawn from Figure 4 on page 341 of D. H. Les (1988), "Hypothetical phylogenetic relationship of Ceratophyllales, Nymphaeales, and modern monocots and dicots." I colorized and changed the font of the typescript to conform to gigantopteroid web page style.

Notes added after-the-fact. Two key papers (Endress and J. A. Doyle 2015, Crepet et al. 2016) appeared in print just following publication of the work discussed above. And further comment on the phylogenetic position of Ceratophyllales in relation to APG III is necessary, in my opinion.

"... What do flowers of living basal angiosperms tell us about the early evolution of flowers? ..." (Introduction on page 1095, Endress and J. A. Doyle 2015).

Little or nothing, if some of the arguments posed by D. H. Les (1988, 1993) and Christianson and Jernstedt (2009) are taken into account. Simply put, the nested reproductive organs seen in species of extant basal flowering plants (Endress and J. A. Doyle 2015) and extinct lauraleans, which are sister to the clade Atherospermataceae + Gomortegaceae (Crepet et al. 2016) exhibit remarkable diversity.

"... Because Amborella, Nymphaeales, and Austrobaileyales (the ANITA groups) form a basal grade of lines that diverge below the vast majority of living angiosperms (the mesoangiosperm clade), they offer a unique opportunity to reconstruct ancestral states in angiosperms and early modifications. However, some characters vary too much among these taxa to identify ancestral states with parsimony ..." (Conclusions on page 1110, Endress and J. A. Doyle 2015).

Yes, especially when considering the flower as a deeply conserved reproductive short shoot with origins from an allopolyploid nexus of late Paleozoic seed plant populations.

Crepet, W. L., K. C. Nixon, D. Grimaldi, and M. Riccio. 2016. A mosaic Lauralean flower from the early Cretaceous of Myanmar. American Journal of Botany 103: 290-297.

Endress, P. K. and J. A. Doyle. 2015. Ancestral traits and specializations in the flowers of the basal grade of living angiosperms. Taxon 64(6): 1093-1116.



Bayesian Computational Molecular Simulations Support a Triassic Age Estimate for Angiosperms (September 2015):

Oxford Journals reports yet another significant molecular-phylogenetic analysis estimating the timing of the origin of angiosperms.

Beaulieu, J. M., B. C. O'Meara, P. R. Crane, and M. J. Donoghue. 2015. Heterogeneous rates of molecular evolution and diversification could explain the Triassic age estimate for angiosperms. Systematic Biology 64(5): 869-878.

Popular accounts of earlier analyses by Stephen A. Smith et al. (2010) were published in the Science Daily, and by Yale University Professor Michael Donoghue.

Students have ample opportunities to compare and contrast Bayesian relaxed-clock methods and to discuss Yule birth-death priors when comparing angiosperm and seed plant phylogenies computed by Bell et al. (2005, 2010), Stephen A. Smith et al. (2010), Magallón (2010, 2014), and Magallón et al. (2015), among others, with the Professor Charles Marshall analyses (Condamine et al. 2015).

Appropriate choice of priors during the course of Bayesian molecular-clock simulations affects estimates on the age of cycad clade branches (Condamine et al. 2015). Birth-death priors, when used in molecular-phylogenetic simulations are more congruent with the fossil record of ancient groups (older-diverging clades) than Yule techniques, and this observation holds true for other biological groups (Condamine et al. 2015).

The fossil record of flowering plants is grossly incomplete despite an optimistic appraisal by Friis et al. (2011). Every one of the simulations computed by Beaulieu et al. (2015) suggest a Triassic age for angiosperms, which is consistent with a growing body of paleontological evidence. More field- and laboratory work is needed with focus on rock layers Permo-triassic in age to find and describe fossils of reproductive spur- [short-] shoots, and detached and shed angiospermous organs and foliar remains.

Paleobotanical data (Cornet 1986, 1989, Cornet and Habib 1992, Cornet 1993), which are challenged and marginalized by certain colleagues, are concordant with some of the mathematical predictions and spin-offs from simulations published by Stephen A. Smith et al. (2010) and Beaulieu et al. (2015).

Paleobiological implications of Bayesian molecular-clock simulations. There is little doubt that Bayesian computational molecular-clock simulations confirm palynological evidence positing several flowering plant populations in arid, boreal, and tropical environments in Anisian times and places (Hochuli and Feist-Burkhardt 2004, 2013). Paleoecologies of these ancient angiosperm populations were not "dark and disturbed," or "wet and wild," or explainable by any other nonsensical pairing of adjectives.

Definitive paleontological evidence published by Peter Hochuli and Susanne Feist-Burkhardt should be read together with a Sidney Ash and Stephen Hasiotis review of Sanmiguelia paleobiology, and their report of three new localities from the Blue Mesa Member (Norian) of the Lower Triassic Chinle Formation of southwestern North America.

Crane (1985) suggested that some populations of late Paleozoic Vojnovskyales might have survived the end-Permian extinction reappearing in the Triassic rock record as the seed plant Sanmiguelia. Does this overlooked and thoughtful comparison merit further exploration? Yes.

"The male structures [of Sanmiguelia] appear to be strobili with sessile pairs of pollen sacs, more reminiscent of ginkgophytes than angiosperms, and the smooth monosulcate pollen has no angiosperm features" (page 319, J. A. Doyle 2012).

Was Sanmiguelia lewisii a stem group angiosperm? Possibly, but this determination must be validated by way of paleobotanical evidence yet to be mined from the rocks. The problem is also semantic as expressed in conflicting opinions on the definition of angiosperms, flowers, and from opposing ideas on supposed character homologies with organs of Paleozoic seed plants.

Homologies of nested structures of reproductive short- [spur]-shoots of Ginkgo with Magnolia floral organs require further study, in my opinion. Despite vigorous defense by J. A. Doyle of Caytoniales as basal to angiosperms in several so-called "combined morphological- and molecular-phylogenetic analyses," this group of pteridosperms is irrelevant toward our understanding of the origin of flowering plants and evolutionary relationships with cone-bearing seed plants. Caytoniales have been (and continue to be) a controversial seed plant group with dubious evolutionary ties to flowering plants.

Paleobotanical data, when subjected to phylogenetic tests for heterochrony (Hufford 1997, 2001) might prove an angiosperm morphological chronocline linking certain Vojnovskyales, through a transitional species such as Sanmiguelia lewisii, to some of the monocotyledonous flowering plants known from the Cretaceous rock record reviewed in Table 1 on pages 349-352 by Iles et al. (2015).

Simply put, wide-ranging Permo-carboniferous Vojnovskyales and relatively abundant Triassic Sanmiguelia should no longer be excluded from seed plant data sets and combined morphological- and molecular-phylogenetic analyses. In fact, Sanmiguelia lewisii should now be used in fossil calibration of monocotyledonous tool kit phylogenies.

Magallón et al. (2015) excluded the Triassic fossil Sanmiguelia lewisii (see the blue-bars on Figure 1) from the angiosperm molecular-phylogenetic analysis, ignoring possibly severe repercussions on calibration of the angiosperm radiation.

Yet, there are incongruencies in a milestone phylogenomic analysis of 1468 single-copy insect nuclear genes by the Bernhard Misof team (cited and discussed on another page) with reanalyses of the data by K. Jun Tong et al. (2015) employing Bayesian priors and fine-tuning node calibrations with fossils, which parallel problems with competing analyses of seed plant molecular data sets discussed by Beaulieu et al. (2015), Condamine et al. (2015), and Magallón et al. (2015), especially when paleontological considerations are included in tree-thinking.

"... we estimate the ages of the megadiverse orders Diptera [flies] and Lepidoptera [butterflies and moths] at ≈266 and ≈263 Ma [million years ago], respectively. These are ≈100 My [million years] earlier than those of Misof et al. [2014]. Our estimates are consistent with the fossil record ... and challenge the hypothesis that these two orders diversified contemporaneously with angiosperms" (quoted from K. Jun Tong et al. 2015, words in brackets [] are mine).

Evolutionary-developmental implications of Bayesian molecular-clock simulations. Almost every molecular-phylogenetic study of DNA-binding seed plant transcription factors (TFs) suggests deep conservation of the cone and floral tool kit. This fact is congruent with Bayesian molecular-clock simulations computed by Beaulieu et al. (2015) supporting Triassic age estimates for flowering plants.

Rate Scenario 3 depicted in Figure 4 on page 874 of Beaulieu et al. (2015) is particularly intriguing from the research perspective of evolutionary-development (evo-devo). For example, there are studies in the paleobotanical and physiological literature on the evo-devo of auxin regulation (Rothwell and Lev-Yadun 2005, Rothwell et al. 2008). Further, auxin-based polarity networks (PINs) of the seed plant shoot apical meristem (SAM) are deeply-conserved.

Based on gene expression studies of extant angiosperm species does the foliar morphology, stem anatomy, and growth habit of Sanmiguelia lewisii display the fingerprint of an "ancestral developmental tool kit" (title, Floyd and Bowman 2007) of a monocotyledonous flowering plant? Yes.

What of magnoliid (and/or eudicot) reproductive spur-shoot and foliar evo-devo, or co-option of the molecular tool kit to generate opposing morphologies of the vegetative leaf subtending the short shoot? And is the reproductive spur-shoot the very same organ as the flower? Yes, if developmental- and scaling-data published by Christianson and Jernstedt (2009) are taken at face value.

Clues may be found in biochemical studies by Bilsborough et al. (2011) of the extant malvid model species, Arabidopsis thaliana. Reverse flows of auxin being drained by leaf midveins have been detected in living foliar organs, and bidirectional hormone flow affects the shape of developing leaves (see Figure 5 on page 3427, Bilsborough et al. 2011). Modeling of auxin gradients in embryonic leaves posits repression of cup-shaped cotyledon-two (CUC2) TFs by the phytohormone auxin as the basis of leaf-margin sculpting (Bilsborough et al. 2011).

Were these deeply-conserved tool kit interactions between auxin, homeodomain protein TFs (CUC2, Class III HD-Zips, KNOX, WUSCHEL), and PIN proteins, present in foliar organs and shoots of Paleozoic seed plants? Possibly, but more work is needed to answer these and other related questions.

Leaf-margin sculpting in Permian Delnortea abbottiae, Evolsonia texana, and associated taeniopteroid "tepal" apexes (i.e. the morphotype Taeniopteris sp.) suggests auxin regulation of ancient CUC2 TFs. Paleobotanical study of the leaf-vein anatomy and leaf-sinus and foliar-apex morphologies of delnorteas, evolsonias, and taeniopteroid "tepals" is needed to support this idea. It will also be important to determine shoot morphologies of these Permian seed plants.

Does the foliar morphology and leaf-midrib anatomy of Permian delnorteas display the developmental fingerprint of a magnoliid or eudicot molecular tool kit. Possibly.

Based on the extensive literature on floral evo-devo, Bayesian relaxed-clock molecular simulations, and palynological evidence, there seems to be diminishing support for Professor James A. Doyle's widely discussed points of view that appear in three significant and profusely-cited reviews published in 1978, 1994, and 2012.

Beginning with a classic 1978 review by J. A. Doyle on the origin of flowering plants, specific arguments subject to differing interpretation include, (1) choice of seed plant character polarities for certain organs and structures (ovules, pollen, ray parenchyma, reproductive SAMs), (2) imputing an unproven chronocline of derived floral organs with supposedly ancestral pteridosperm cupules inconsistent with fundamentals of seed plant SAM evo-devo, and (3) over-reliance of the bitegmic ovule as an angiosperm-specific character.

Equally perplexing is an apparent misunderstanding by some paleobotanists of SAM evo-devo, specifically the importance of molecular tool kits consisting of DNA-binding homeodomain proteins, cis-regulatory modules (CRMs), gene-regulatory networks (GRNs), and hormone polarity networks (PINs), which are necessary for the evo-devo of flowers and reproductive short- [spur-] shoots.

Some morphologists and paleobotanists might be misinterpreting certain aspects of seed plant ovule growth and development including integumentary fusion and splitting, which is inherently plastic. At least one modern synthesis (Endress 2015) may be helpful in understanding these problems, among others. These are but few of problems leading to dubious conclusions on floral homologies.

Concluding remarks. Students and researchers should not forget that the first clue shedding light on the shadowy origin of flowering plants is from geochemical study of taxon-specific biomarkers (TSBs). These molecular tracers are recoverable from mud logs of well boreholes (Moldowan and Jacobson 2002), which are widely used by the oil and gas industry to pin-point sedimentary rocks having terrestrial fossil seed plant input.

Compounding the problems listed in the previous section is a notable lack of enthusiasm by certain workers, recognizing important oleonone triterpane TSBs left behind in the sedimentary rock record, as evidence for the existence of Permo-carboniferous angiosperm populations. When considered together with results of early molecular studies of proteins, and modern phytochrome molecular-phylogenetic analyses suggesting a late Paleozoic origin of angiosperms, oleananes detected in Permo-carboniferous rocks are an "inconvenient truth."

Some paleobotanists reject Sanmiguelia lewisii as a stem-group angiosperm and eliminate Vojnovskyales and sanmiguelias from so-called combined morphological- and molecular-phylogenetic analyses (J. A. Doyle 2001, 2006, 2008). Dubious arguments posed by J. A. Doyle and Endress (2014) on the importance of exine thickness to discredit Triassic angiosperm pollen records (Afropollis and angiosperm-like pollen from Anisian sedimentary layers possesses thin exine) are equally perplexing, in my opinion.

Yet, some paleobotanists have yet to embrace the concept of the flower as a deeply-conserved seed plant organ. According to Christianson and Jernstedt (2009) the flower is homologous with the Ginkgo reproductive short- [spur-] shoot. Reproductive short- [spur-] shoots, composed of spirally-arranged tepals and nested sporophylls, are discernable in the fossil record of Permo-carboniferous Vojnovskyales, and other ancient gymnosperm groups, including cycads, ginkgophytes, and gnetophytes. These organs should be viewed as "protoflowers," which is a classical concept first proposed by Arber and Parkin (1907) and Leppik (1960, 1968).

Further, the well-reasoned and classical papers on seed plant evolution and the origin of angiosperms (J. A. Doyle and Donoghue 1986, 1987) were apparently abandoned prematurely following discovery of Amborella trichopoda at the base of the flowering-plant phylogenetic tree, more than a decade later.

Studies of the genomic landscape of Amborella trichopoda are probably unhelpful in discerning angiosperm stem groups of Permo-triassic times and places, proving intergeneric hybridization in ancient zones of sympatry, and elucidating reproductive mechanisms leading to allopolyploid formation and dispersal of hybrid offspring. Misunderstood Late Paleozoic gigantopteroids and Vojnovskyales might be important in elucidating the origin of angiosperms.

Several questions surface from molecular-clock simulations published by Stephen A. Smith et al. (2010) and Beaulieu et al. (2015):

Are the Beaulieu et al. molecular-phylogenetic simulations pictured in Figures 3 and 4, estimating the age of angiosperm stem group populations consistent with paleobotanical- and palynological evidence. Yes.

Paleobotanical data including future studies of reproductive SAM- and leaf-theoretical morphospace might someday demonstrate that woody gigantopteroids (delnorteas and evolsonias) and species of Vojnovskyales are the ancestors of flowering plants. Further, sanmiguelias could be direct descendents of Vojnovskyales that survived the end-Permian extinction. If true, the concluding statement on page 876 of Beaulieu et al. (2015) would be even more predictive.

"... The shifts in plant habit and molecular rate that actually occurred in the course of angiosperm evolution will have been far more complicated than we have represented in our simulations ..."

Should it be demonstrated that Vojnovskyales are direct ancestors of angiosperms, and taking into account concatenated molecular-phylogenetic analyses of seed plants suggesting that flowering plants are sister to conifers, cycads, ginkgophytes, and gnetophytes (Mathews 2009), then how can pteridosperms possibly comprise "the backbone of seed-plant evolution" (Title, Hilton and Bateman 2006)?

If Triassic flowering plant populations were broadly distributed across the Pangaean continent (they were, based on palynological evidence), is a late Paleozoic origin of angiosperms likely?

The study by Beaulieu et al. (2015) is remarkable because its mathematical precision and sophisticated computational molecular-clock simulations open a new window illuminating an old problem. Paleobiologists may now focus on rock layers Triassic or Permian in age to find fossils that belong to the angiosperm stem group including detached remains of foliar organs representing developmental fingerprints of novel CRMs, GRNs, and PINs of reproductive short shoots comprising the oldest protoflowers.

"Under the circumstances, it behooves us to remain humble and to honestly assess potential biases not only in the fossil record, but also in our methods for analyzing molecular data" (page 876, Beaulieu et al. 2015).

I conclude that a swarm of seed plant whole genome duplications (WGDs) in the late Paleozoic Era modeled by Jiao et al. (2011) was a result of intergeneric hybridization, possibly insect-mediated, and classic allopolyploidy at the base of the angiosperm tree.

References:

Arber, E. A. N. and J. Parkin. 1907. On the origin of angiosperms. Botanical Journal of the Linnaean Society 38: 28-80.

Ash, S. R. and S. T. Hasiotis. 2013. New occurrences of the controversial late Triassic plant fossil Sanmiguelia Brown and associated ichnofossils in the Chinle Formation of Arizona and Utah, USA. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 268(1): 65-82.

Beaulieu, J. M., B. C. O'Meara, P. R. Crane, and M. J. Donoghue. 2015. Heterogeneous rates of molecular evolution and diversification could explain the Triassic age estimate for angiosperms. Systematic Biology 64(5): 869-878.

Bell, C. D., D. E. Soltis, and P. S. Soltis. 2005. The age of the angiosperms: a molecular timescale without a clock. Evolution 59(6): 1245-1258.

Bell, C. D., D. E. Soltis, and P. S. Soltis. 2010. The age and diversification of the angiosperms revisited. American Journal of Botany 97: 1296-1303.

Bilsborough, G. D., A. Runions, M. Barkoulas, H. W. Jenkins, A. Hasson, C. Galinha, P. Laufs, A. Hay, P. Prusinkiewicz, and M. Tsiantis. 2011. Model for regulation of Arabidopsis thaliana leaf margin development. Proceedings of the National Academy of Sciences 108(8): 3424-3429.

Christianson, M. L. and J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: a quantitative analysis of the disposition of axillary structures. American Journal of Botany 96(11): 1957-1966.

Condamine, F. L., N. S. Nagalingum, C. R. Marshall, and H. Morlon. 2015. Origin and diversification of living cycads: a cautionary tale on the impact of the branching process prior to Bayesian molecular dating. BMC Evolutionary Biology 15: 65.

Cornet, B. 1986. The leaf venation and reproductive structures of a late Triassic angiosperm, Sanmiguelia lewisii. Evolutionary Theory 7: 231-309.

Cornet, B. 1989. The reproductive morphology and biology of Sanmiguelia lewisii, and its bearing on angiosperm evolution in the late Triassic. Evolutionary Trends in Plants 3(1): 25-51.

Cornet, B. 1989. Late Triassic angiosperm-like pollen from the Richmond Rift Basin of Virginia. Palaeontographica B 213: 37-87.

Cornet, B. 1993. Dicot-like leaf and flowers from the Late Triassic tropical Newark Supergroup Rift Zone, U.S.A. Modern Geology 19: 81-99.

Cornet, B. and D. Habib. 1992. Angiosperm-like pollen from the ammonite-dated Oxfordian (Upper Jurassic) of France. Review of Palaeobotany and Palynology 71: 269-294.

Crane, P. R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanic Garden 72: 716-793.

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Doyle, J. A. 1994. Origin of the angiosperm flower: a phylogenetic perspective. Plants Systematics and Evolution (Supplement) 8: 7-29.

Doyle, J. A. 2001. Significance of molecular phylogenetic analyses for paleobotanical investigations on the origin of angiosperms. The Palaeobotanist 50: 167-188.

Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. The Journal of the Torrey Botanical Society 133(1): 169-209.

Doyle, J. A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169(7): 816-843.

Doyle, J. A. 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40: 301–326.

Doyle, J. A. and M. J. Donoghue. 1986. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Botanical Review (Lancaster) 52(4): 321-431.

Doyle, J. A. and M. J. Donoghue. 1987. The origin of angiosperms: a cladistic approach.  Pp. 17-49 in: E. M. Friis, W. G. Chaloner, and P. R. Crane, The Origin of Angiosperms and Their Biological Consequences.  Cambridge: Cambridge University Press, 358 pp.

Doyle, J. A. and P. K. Endress. 2014. Integrating early Cretaceous fossils into the phylogeny of living angiosperms: ANITA lines and relatives of Chloranthaceae. International Journal of Plant Sciences 175(5): 555-600 (with supplements).

Endress, P. K. 2015. Patterns of angiospermy development before carpel sealing across living angiosperms: diversity, and morphological and systematic aspects. Botanical Journal of the Linnean Society 178: 556-591.

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Friis, E. M., P. R. Crane, and K. R. Pedersen. 2011. Early Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press, 596 pp.

Hilton, J. and R. M. Bateman. 2006. Pteridosperms are the backbone of seed-plant evolution. Journal of the Torrey Botanical Society 133(1): 119-168.

Hochuli, P. A. and S. Feist-Burkhardt. 2004. A boreal early cradle of angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). Journal of Micropalaeontology 23: 97-104.

Hochuli, P. A. and S. Feist-Burkhardt. 2013. Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (Northern Switzerland). Frontiers in Plant Science, Plant Evolution and Development 4: Article 344.

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Hufford, L. 2001. 2. Ontogenetic sequences: homology, evolution, and the patterning of clade diversity. Pp. 27-57 In: M. L. Zelditch (ed.), Beyond heterochrony: the evolution of development. Wiley, New York.

Iles, W. J. D., Selena Y. Smith, M. A. Gandolfo, and Sean W. Graham. 2015. Monocot fossils suitable for molecular dating analyses. Botanical Journal of the Linnean Society 178: 346-374.

Jiao, Y., N. L. Wickett, S. Ayyampalayam, A. S. Chanderbali, L. Landherr, P. E. Ralph, L. P. Tomsho, Y. Hu, H. Liang, P. S. Soltis, D. E. Soltis, S. W. Clifton, S. E. Schlarbaum, S. C. Schuster, H. Ma, J. Leebens-Mack, and C. W. dePamphilis. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345): 97-100.

Leppik, E. E. 1960. Early evolution of flower types. Lloydia 23(3): 72-92.

Leppik, E. E. 1968. Directional trend of floral evolution. Acta Biotheoretica 18A(1-4): 87-102.

Magallón, S. 2010. Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Systematic Biology 59(4): 384-399.

Magallón, S. 2014. A review of the effect of relaxed clock method, long branches, genes, and calibrations in the estimation of angiosperm age. Botanical Sciences (Boletín de la Sociedad Botánica de México) 92[1]: 1-22.

Magallón, S., S. Gómez-Acevedo, L. L. Sánchez-Reyes, and T. Hernández-Hernández. 2015. A meta-calibrated time tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist 207: 437-453.

Mathews, S. 2009. Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. American Journal of Botany 96(1): 228-236.

Moldowan, J. M. and S. R. Jacobson. 2002. Chemical signals for early evolution of major taxa: biosignatures and taxon-specific biomarkers. Pp. 19-26 In: W. G. Ernst (ed.), Frontiers in Geochemistry, Organic, Solution, and Ore Deposit Geochemistry, Konrad Krauskopf Volume 2, International Book Series, Volume 6. Columbia: Bellwether Publishing Ltd., 265 pp.

Rothwell, G. W. and S. Lev-Yadun. 2005. Evidence of polar auxin flow in 375 million-year-old fossil wood. American Journal of Botany 92: 903-906.

Rothwell, G. W., H. Sanders, S. E. Wyatt, and S. Lev-Yadun. 2008. A fossil record for growth regulation: the role of auxin in wood evolution. Annals Missouri Botanical Garden 95: 121-134.

Smith, Stephen A., J. M. Beaulieu, and M. J. Donoghue. 2010. An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proceedings of the National Academy of Sciences 107(13): 5897-5902.

Tong, K. Jun, S. Duchêne, S. Y. W. Ho, and N. Lo. 2015. Comment on "Phylogenomics resolves the timing and pattern of insect evolution." Science 349(6247): Research Technical Comment Number 487, Insect Phylogenomics.

I thank Rudolf Schmid, Ph.D. for bringing to my attention little known and often overlooked pioneering work by Leppik, among others. The extensive Schmid library, including books, card index, and reprints, is now housed at the New York Botanical Garden.



Flower Fossil Posits a Jurassic Angiosperm Crown Bedeviling Doctrine and Confounding Phylogenies (March 2015):

The Xin Wang Laboratory and Nanjing Institute of Geology and Palaeontology reports yet another significant find of a demonstrably ancient flower from the Callovian (or Oxfordian) Jiulongshan Formation (Middle-Late Jurassic), 161.8 MYA, based on the chronostratigraphic analyses by S-C. Chang et al. (2014).

Liu, Z-J. and Xin Wang. 2015. A perfect flower from the Jurassic of China. Historical Biology: An International Journal of Paleobiology DOI: 10.1080/8912963.2015.1020423.

The drawing to the left is Euanthus panii (family uncertain, order not yet assigned, Magnolianae). Artist's reconstruction is reproduced with the written permission of Xin Wang, Nanjing Institute of Geology and Palaeontology, copyright ©2015, all rights reserved.

Several vexing questions surface from this astounding paleobotanical discovery:

Paleohexaploidy i.e. the gamma (γ)- triplication at the heart of the radiation of eudicots (Jiao et al. 2012) is apparently absent in the evolutionary history of the New Caledonian endemic species Amborella trichopoda according to the studies cited elsewhere. From the research perspective of developmental regulation of the floral tool kit was Euanthus panii a paleohexaploid core eudicot or rosid existing in times and places, Jurassic in age?

Is the single paleopolyploid event discerned from study of the Amborella genome including an epsilon (ε)- whole genome duplication (WGD), which is depicted as the asterisk in the figured Structured Abstract of Amborella Genome Project (2013), part of the ancient alpha (α)- swarm of WGDs modeled by Jiao et al. (2011)?

Do arguments published by Friis et al. (2011) and J. A. Doyle (2012) on a Hauterivian origin of the angiosperm crown group, including evo-devo and phylogenetic significance of bitegmic ovules and supposed homologies with pteridosperm cupules, hold water any longer?

Can ategmic ovules develop by fusion of integuments? Yes, according to R. H. Brown et al. (2010).

Is the bitegmic ovule an angiosperm-specific character? No.

Angiosperm ghost lineage. From a fundamental molecular tool kit research perspective flowering plants could be paraphyletic. The advanced floral bauplan of Euanthus panii predates Lesqueria elocata and other magnoliids in the stratigraphic column by more than 20 million years leaving open the possibility of an older and more highly-branched angiosperm crown phylogeny than suggested by Friis et al. (2011) and J. A. Doyle (2012).

Further, whole genome duplications including the γ-triplication probably resulted from interspecific hybridization and classic allopolyploidy in paleopopulations of genetically unrelated evolutionary lines.

Based on "fingerprints of developmental regulation" (quoted from page 723, Sanders et al. 2007), are there examples of fossilized reproductive short- [spur-] shoots, including component but subtending megaphylls, representing monocot and magnoliid floral tool kits, respectively, known from Permo-triassic or Permo-carboniferous rocks? Possibly.

How can a single ancestral Amborella trichopoda genome be manifest "throughout angiosperm history" (Structured Abstract Discussion, Amborella Genome Project 2013) without genetic input from unrelated seed plant populations? It probably cannot, if the species is a paleopolyploid.

Should students of evo-devo recompute a combined morphological- and molecular phylogenetic analysis of flowering plants to reflect extreme conservation of the floral tool kit and to incorporate allopolyploidy at the base of the angiosperm stem(s)? Yes.

The drawing to the right is Lesqueria elocata (family uncertain, Magnoliales, Magnolianae) from page 399 of Crane and Dilcher (1984), Lesqueria: an early angiosperm fruiting axis from the mid-Cretaceous, Annals of the Missouri Botanical Garden 71(2): 384-402, reproduced by permission from Peter Crane, David Dilcher, and the Missouri Botanical Garden.

"Figure 47. Reconstruction of the Lesqueria elocata fruiting axis."

According to Glover et al. (2015), the flower is a relatively recent evolutionary innovation. Based on the deeply-conserved molecular tool kit, what is a flower?

When in Geologic Time did the first flowers bloom?

From the perspective of a plant population ecologist or systematist, is this second question stated with precision?

Morphological evidence suggests that reproductive male and female spur shoots of "living fossil" ginkgos are homologous with angiosperm flowers (Christianson and Jernstedt 2009). In view of these morphological studies, the first question posed above is academic. Consequently, hypotheses on origins of angiosperms and flowers proposed by J. A. Doyle (1978, 1994) are incorrect, and the debate in paleobotanical circles on possible ginkgoalean affinities of Schmeissneria is superfluous.

Taking into account homologies of the floral organ with certain gymnosperm reproductive short- [spur-] shoots, how can flowers constitute evolutionary novelties? They cannot, based on examples of reproductive short- [spur-] shoots (possible protoflowers) found preserved in Permo-carboniferous rocks.

Should further study including whole plant reconstructions and computation of floral morphospace demonstrate that Euanthus panii constitutes a crown group angiosperm (cursory evaluation of the fossil by any plant morphologist, systematist, or paleobotanist would support this assessment), how would fossil calibration affect the chronology of core eudicot diversification on coauthored Beaulieu, Bell, Soltis, and Magallón molecular-phylogenetic analyses based on APG III data and certain priors?

Paleobotanical and palynological evidence of a 160 million year old angiosperm ghost lineage rooted at the angiosperm-gymnosperm split more than 250 MYA, prior to the end-Permian extinction is mounting. There are too many credible reports of pre-Hauterivian flowering plants in the peer-reviewed paleontological literature to be marginalized by certain colleagues (specified from the literature since 1978, and the curious statement, quoted below), some journal editors, and writers of book chapters and textbooks:

"Some authors seem curiously determined to prove that pre-Cretaceous fossils are crown-group angiosperms, but for understanding most aspects of the origin of angiosperms [other than their age], close stem relatives would be far more significant" (page 318, J. A. Doyle 2012).

Flowering plants are sister to conifers, cycads, ginkgophytes, and gnetophytes in several molecular phylogenetic analyses of seed plants (Mathews 2009). Fossil pollen studies point to several possible Triassic flowering plant populations in arid, boreal, and tropical environments (Hochuli and Feist-Burkhardt 2013).

Paleontological evidence published by Cornet, Hochuli and Feist-Burkhardt, and Xin Wang and coworkers calls in question a whole body of paleophysiologic work on the ecologies of so-called "early" angiosperms.

Some of provisionally-classified "Gymnosperms With Obscure Affinities" discussed in Chapter 19 on page 757 of T. N. Taylor et al. (2009) might be evolutionarily precocious novelties with reproductive short-[spur] shoots and dimorphic leaves, representing hybridizing seed plant populations at the base of the angiosperm stem.

Delnorteas and evolsonias, which are neither Auritifolia waggoneri or Supaia thinnfeldioides peltasperms, and Vojnovskyales (including Triassic sanmiguelias) fit this bill. Granting agencies, established laboratories, and organizers of symposia should consider these possibilities, in my opinion.

Further, the statement by Wing and Boucher (page 380, 1998) is probably incorrect: "Despite the singular ecological significance and species diversity of angiosperms, they are not in a genealogical sense one of the major branches of land plants and did not originate with other major land plant clades (e.g. lycopsids, ferns, conifers, cycads, ginkgos) during the middle or late Paleozoic."

References:

Amborella Genome Project. 2013. The Amborella genome and the evolution of flowering plants. Science 342(6165): 1467.

Bell, C. D., D. E. Soltis, and P. S. Soltis. 2005. The age of the angiosperms: a molecular timescale without a clock. Evolution 59(6): 1245-1258.

Bell, C. D., D. E. Soltis, and P. S. Soltis. 2010. The age and diversification of the angiosperms revisited. American Journal of Botany 97: 1296-1303.

Bomfleur, B., A-L. Decombeix, A. B. Schwendemann, I. H. Escapa, E. L. Taylor, T. N. Taylor, and S. McLoughlin. 2014. Habit and ecology of the Petriellales, an unusual group of seed plants from the Triassic of Gondwana. International Journal of Plant Sciences 175(9): 1062-1075.

Brown, R. H., Nickrent, D. L. and C. S. Gasser. 2010. Expression of ovule and integument-associated genes in reduced ovules of Santalales. Evolution and Development 12(2): 231-240.

Chang, S-C., H. Zhang, S. R. Hemming, G. T. Mesko, and Y. Fang. 2014. 40Ar/39 age constraints on the Haifanggou and Lanqi formations. Geological Society of London Special Publication 378(1): 277-284.

Christianson, M. L. and J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: a quantitative analysis of the disposition of axillary structures. American Journal of Botany 96(11): 1957-1966.

Cornet, B. 1986. The leaf venation and reproductive structures of a late Triassic angiosperm, Sanmiguelia lewisii. Evolutionary Theory 7: 231-309.

Cornet, B. 1989. The reproductive morphology and biology of Sanmiguelia lewisii, and its bearing on angiosperm evolution in the late Triassic. Evolutionary Trends in Plants 3(1): 25-51.

Cornet, B. 1989. Late Triassic angiosperm-like pollen from the Richmond Rift Basin of Virginia. Palaeontographica B 213: 37-87.

Cornet, B. 1993. Dicot-like leaf and flowers from the Late Triassic tropical Newark Supergroup Rift Zone, U.S.A. Modern Geology 19: 81-99.

Cornet, B. and D. Habib. 1992. Angiosperm-like pollen from the ammonite-dated Oxfordian (Upper Jurassic) of France. Review of Palaeobotany and Palynology 71: 269-294.

Doyle, J. A. 1978. Origin of Angiosperms. Annual Review of Ecology and Systematics 9: 365-392.

Doyle, J. A. 1994. Origin of the angiosperm flower: a phylogenetic perspective. Plants Systematics and Evolution (Supplement) 8: 7-29.

Doyle, J. A. 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40: 301–326.

Doyle, J. A. 2015. Recognising angiosperm clades in the Early Cretaceous fossil record. Historical Biology: An International Journal of Paleobiology 27(3-4): 414-429.

Friis, E. M., P. R. Crane, and K. R. Pedersen. 2011. Early Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press, 596 pp.

Hochuli, P. A. and S. Feist-Burkhardt. 2004. A boreal early cradle of angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). Journal of Micropalaeontology 23: 97-104.

Hochuli, P. A. and S. Feist-Burkhardt. 2013. Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (Northern Switzerland). Frontiers in Plant Science, Plant Evolution and Development 4: Article 344.

Jiao, Y., J. Leebens-Mack, S. Ayyampalayam, J. E. Bowers, M. R. McKain, J. McNeal, M. Rolf, D. R. Ruzicka, E. Wafula, N. L. Wickett, X. Wu, Yong Zhang, J. Wang, Yeting Zhang, E. J. Carpenter, M. K. Deyholos, T. M. Kutchan, A. S. Chanderbali, P. S. Soltis, D. Wm. Stevenson, R. McCombie, J. C. Pires, G. K.-S. Wong, D. E. Soltis, and C. W. dePamphilis. 2012. A genome triplication associated with early diversification of eudicots. Genome Biology 13: R3.

Jiao, Y., N. L. Wickett, S. Ayyampalayam, A. S. Chanderbali, L. Landherr, P. E. Ralph, L. P. Tomsho, Y. Hu, H. Liang, P. S. Soltis, D. E. Soltis, S. W. Clifton, S. E. Schlarbaum, S. C. Schuster, H. Ma, J. Leebens-Mack, and C. W. dePamphilis. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345): 97-100.

Liu, Z-J. and Xin Wang. 2015. A perfect flower from the Jurassic of China. Historical Biology: An International Journal of Paleobiology DOI: 10.1080/8912963.2015.1020423.

Magallón, S. 2010. Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Systematic Biology 59(4): 384-399.

Magallón, S. 2014. A review of the effect of relaxed clock method, long branches, genes, and calibrations in the estimation of angiosperm age. Botanical Sciences (Boletín de la Sociedad Botánica de México) 92[1]: 1-22.

Mathews, S. 2009. Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. American Journal of Botany 96(1): 228-236.

Misof, B., Shanlin Liu, K. Meusemann, R. S. Peters, A. Donath, C. Mayer, P. B. Frandsen, J. Ware, T. Flouri, R. G. Beutel, O. Niehuis, M. Petersen, F. Izquierdo-Carrasco, T. Wappler, J. Rust, A. J. Aberer, U. Aspöck, H. Aspöck, D. Bartel, A. Blanke, S. Berger, A. Böhm, T. R. Buckley, B. Calcott, Junqing Chen, F. Friedrich, M. Fukui, M. Fujita, C. Greve, P. Grobe, Shengchang Gu, Ying Huang, L. S. Jermiin, A. Y. Kawahara, L. Krogmann, M. Kubiak, R. Lanfear, H. Letsch, Yiyuan Li, Zhenyu Li, Jiguang Li, Haorong Lu, R. Machida, Y. Mashimo, P. Kapli, D. D. McKenna, Guanliang Meng, Y. Nakagaki, J. L. Navarrete-Heredia, M. Ott, Yanxiang Ou, G. Pass, L. Podsiadlowski, H. Pohl, B. M. von Reumont, K. Schütte, K. Sekiya, S. Shimizu, A. Slipinski, A. Stamatakis, Wenhui Song, Xu Su, N. U. Szucsich, Meihua Tan, Xuemei Tan, Min Tang, Jingbo Tang, G. Timelthaler, S. Tomizuka, M. Trautwein, Xiaoli Tong, T. Uchifune, M. G. Walz, B. M. Wiegmann, J. Wilbrandt, B. Wipfler, T. K. F. Wong, Qiong Wu, Gengxiong Wu, Yinlong Xie, Shenzh Yang, D. K. Yeates, K. Yoshizawa, Qing Zhang, Rui Zhang, Wenwei Zhang, Yunhui Zhang, Jing Zhao, Chengran Zhou, Lili Zhou, T. Ziesmann, Shijie Zou, Yingrui Li, Xun Xu, Yong Zhang, Huanming Yang, Jian Wang, Jun Wang, K. M. Kjer, and Xin Zhou. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346(6210): 763-767.

Sanders, H., G. W. Rothwell, and S. E. Wyatt. 2007. Paleontological context for the developmental mechanisms of evolution. International Journal of Plant Sciences 168: 719-728.

Taylor, T. N., E. L. Taylor, and M. Krings. 2009. Paleobotany: The Biology and Evolution of Fossil Plants, Second Edition. Burlington: Elsevier Academic Press, 1230 pages.

Tong, K. Jun, S. Duchêne, S. Y. W. Ho, and N. Lo. 2015. Comment on "Phylogenomics resolves the timing and pattern of insect evolution." Science 349(6247): 487.

Wang, Xin. 2009. New fossils and new hope for the origin of angiosperms. Pp. 51-70 In: P. Pontarotti (ed.), Evolutionary biology: Concept, Modeling, and Application. London: Springer Verlag, 398 pp.

Wang, Xin. 2014. The megafossil record of early angiosperms in China since 1930s. Historical Biology: An International Journal of Paleobiology, DOI: 10.1080/08912963.2014.889695.

Wang, Xin, S. Duan, B. Geng, J. Cui, and Y. Yang. 2007. Schmeissneria: A missing link to angiosperms? BMC Evolutionary Biology 7: 14-26.

Wang, Xin and S. Wang. 2010. Xingxueanthus: an enigmatic Jurassic seed plant and its implications for the origin of angiospermy. Acta Geologica Sinica 84(1): 47-55.

Concluding remarks. Despite considerable discussion in the literature on angiosperm phylogeny and evolution by J. A. Doyle (2015), among others, the existence of a highly derived flower from Jurassic rocks precludes Caytoniales and Petriellales from having anything to do, whatsoever, with the "mysterious origin of flowering plants" (quoted from page 1074, Discussion, Ecology and Paleoenvironment, Bomfleur et al. 2014).

Since the reproductive branch bauplan of Caytonia is incongruent with most models of cone and floral evo-devo, should paleobotanists dispose of Caytoniales, which are basal to the flowering plant clade in several morphological- and combined morphological-molecular phylogenetic analyses of seed plants?

There is no excuse for scientists and their students to accept botanical, ecological, paleontological, and morphological doctrine when [certain] arguments are based on assumptions or unreliable data, especially in view of widely-available and proven utility of empirical approaches (chronostratigraphy, morphometrics, phylogenetics, proxies, statistics, taphonomy), modern methods of microscopy and tomography (see below), and theoretical approaches incorporating techniques and tenets of evolutionary development (evo-devo), plant physics, and morphospace.

Notes added after-the-fact. Another important installment from the Friis Laboratory on the paleobiology of "early angiosperms" has been published in Nature. The paleobotanical study by Friis et al. (2015) is significant. Details on preservation of seeds, precision of the diagnosis, taphonomy, and stratigraphic control are unequivocal.

Synchrotron radiation tomography of fossilized organs of Anacostia, Appomattoxia, Canrightiopsis, and other indeterminate seeds reveal details of minute embryos not unlike features seen in extant basal flowering plants and more advanced magnoliids including bird dispersed seeds and tiny embryos of Degeneriaceae, which are not reviewed in the letter published by Friis et al. (2015).

On the other hand, details of stratigraphy and taphonomy of the single fossilized and entombed flower described by Z-J. Liu and Xin Wang (2015) and Crepet et al. (2016), respectively, are controversial. Sample history and a chain of custody of Euanthus panii (Z-J. Liu and Xin Wang 2015) and Jamesrosea burmensis (Crepet et al. 2016) is problematic.

There are additional reports of seed plant foliage and reproductive organs published by Xin Wang and co-workers from Middle Jurassic volcaniclastic deposits of the Jiulongshan Formation (Gang Han et al. 2016, Z-J. Liu and Xin Wang 2016). While these fossil finds are interesting, assignment of foliage, fruits, and ovules to a specific group of seed plants is open to differing interpretation.

Dating of the >165 million-year-old rock layers of the Jiulongshan Formation is unequivocal (Table 1 on page 3 of Y.-Q. Liu et al. 2012). Paleobotanists might disagree with certain details of the diagnosis of Juraherba bodae and Yuhania daohugouensis (monocotyledonous flowering plants, incertae cedis).

Gang Han et al. (2016) suggest that Juraherba was a monocotyledonous angiosperm as pivotal in supporting a "Paleoherb Hypothesis" on the origin of flowering plants, but neglect deductive comparison of the fossilized fructification with Cretovarium (Stopes and Fujii 1910) and Mabelia (Gandolfo et al. 2002). William Burger and Bruce Cornet's proposals on the origin and evolution of monocotyledonous angiosperms (Cornet references are listed in the succeeding news clip) are not discussed by Gang Han et al. (2016), which is unfortunate and potentially troubling, in my opinion.

The two latest installments of paleobotanical work by Xin Wang and colleagues offer fodder for comment and discussion. But there are other ways to interpret preserved seed plant parts and whole stem axes and foliar material recovered from layers of the Jiulongshan Formation.

Discussion of anatomical features, supposed chronoclines linking Permo-triassic gymnosperms with magnoliids, and evolutionary relationships of carpels with megasporophylls is necessary to decipher morphologies of Jiulongshan seed plant fossils. Further, our Asian colleagues should discuss the "megasporophyll-homology hypothesis" on page 119 of D. W. Taylor and Kirchner (1996), among other work, to formulate criteria necessary to decipher fossilized fruits.

Serge Mamay (Figure 7, page 33, 1976) was a 20th Century paleobotanist who proposed a conduplicately-folded megasporophyll hypothesis for a Paleozoic origin of Cycadales. Yet, this potentially important and classical hypothesis was not discussed by D. W. Taylor, Kirchner, or Xin Wang, among others. Finally, it might have been helpful for Z-J. Liu and Xin Wang (2016) to cast their discussion of Yuhania fruit anatomy to include comparisons with the Permo-carboniferous seed plant Phasmatocycas bridwellii (Axsmith et al. 2003).

Added References:

Axsmith, B. J., R. Serbet, M. Krings, T. N. Taylor, E. L. Taylor, and S. H. Mamay. 2003. The enigmatic Paleozoic plants Spermopteris and Phasmatocycas reconsidered. American Journal of Botany 90(11): 1585-1595.

Crepet, W. L., K. C. Nixon, D. Grimaldi, and M. Riccio. 2016. A mosaic Lauralean flower from the early Cretaceous of Myanmar. American Journal of Botany 103: 290-297.

Friis, E. M., P. R. Crane, K. R. Pedersen, M. Stampanoni, and F. Marone. 2015. Exceptional preservation in tiny embryos of early angiosperms. Nature 528: 551-555.

Gandolfo, M. A., K. C. Nixon, and W. L. Crepet. 2002. Triuridaceae fossil flowers from the Upper Cretaceous of New Jersey. American Journal of Botany 89(12): 1940-1957.

Han, Gang, Z-J. Liu, X-L. Liu, M. Limi, F. M. B. Jacques, and Xin Wang. 2016. A whole plant herbaceous angiosperm from the Middle Jurassic of China. Acta Geologica Sinica 90(1): 19-29.

Liu, Y.-Q., H.-W. Kuang, X.-J. Xiang, N. Peng, H. Xu, and H.-Y. Sun. 2012. Timing of the earliest known feathered dinosaurs and transitional pterosaurs older than the Jehol Biota. Palaeogeography, Palaeoclimatology, and Palaeoecology 323-325: 1-12.

Liu, Z-J. and Xin Wang. 2016. Yuhania: a unique angiosperm from the Middle Jurassic of Inner Mongolia, China. Historical Biology DOI 10:1080/089112963.2016.1178740.

Mamay, S. H. 1976. Paleozoic Origin of the Cycads. U. S. Geological Survey Professional Paper 934, 48 pp.

Stopes, M. C. and K. Fujii. 1910. Studies on the structure and affinities of Cretaceous plants. Philosophical Transactions of the Royal Society of London. B201: 1-90.

Taylor, D. W. and G. Kirchner. 1996. Chapter 6. The origin and evolution of the angiosperm carpel. Pp. 116-140 In: D. W. Taylor and L. J. Hickey (eds.), Flowering Plant Origin, Evolution, and Phylogeny. London: Chapman and Hall, 403 pp.

I thank Ralph Molnar, Ph.D. for bringing these studies by our Asian colleagues to my attention.



Reproductive Modules and Gametangial Programs in Welwitschia are Gnetalean Synapomorphies (February 2015):

Yet another important study of seed plant development by Bill Friedman illuminates the highly derived reproductive anatomy of Welwitschia mirabilis (Welwitschiaceae, Gnetales, Gnetophyta), including growing prothallial tubes, endoreduplicated nuclei, and single fertilization occurring between the functional sperm nucleus of a pollen tube and one prothallium egg cell. The evolutionary history of modular reproductive development in extant Gnetales is reviewed by Friedman (2015) in two papers.

Friedman, W. E. 2015. Evolving words and the egg-bearing tubes of Welwitschia (Welwitschiaceae). American Journal of Botany 102(2): 176-179.

Friedman, W. E. 2015. Development and evolution of the female gametophyte and fertilization process in Welwitschia mirabilis (Welwitschiaceae). American Journal of Botany 102(2): 312-324.

A photomicrograph of polyplicate gnetalean pollen, which are lodged in the pollen chamber of a permineralized ovule of Eoantha zherikhinii (Gnetales, Gnetophyta), appears on the left side of the news clip, ×1000. The original image was supplied to the author by Professor Valentine Krassilov with permissions, for posting on my web site several years ago.

Prepared permineralized material of Eoantha (Gnetales) including another photomicrograph of this preparation, appears on page 197, Figure 5, Plate 21 of V. A. Krassilov (1997), Angiosperm Origins: Morphological and Ecological Aspects. Sofia: Pensoft, 270 pp. The late Valentine Krassilov once drew connections of gnetalean paleobiology with angiosperms in several published works (1977, 1986, 1991, 1997, 2002, 2009).

What was the nature of the evolutionary "gametangial differentiation program" (page 319, Discussion: Female Gametophyte Character Evolution in Gnetales, Friedman 2015) in certain gnetophyte populations of Transbaikal, or the common ancestors of Gnetum and Welwitschia?

Gnetales are well-represented in the Mesozoic fossil record according to Krassilov (1997), Krassilov and Ash (1988), and Krassilov and Bugdaeva (2000). A morphological-phylogenetic analysis of the often overlooked reproductive organs of Palaeognetaleana, while taking into account molecular-phylogenetic studies by Mathews (2009), and supposed homologies of gnetalean double fertilization with flowering plants, offer fodder for debate and discussion of modular reproductive development in the most recent common ancestor (MRCA).

" ... this pattern of gnetalean double fertilization might well be homologous with the process of double fertilization in angiosperms (Friedman and Floyd 2001). However, a seismic shift in favored phylogenetic hypotheses for seed plants associated with the transition from morphological cladistic analyses to DNA sequence-based analyses indicated (and continues to indicate-see above) that Gnetales are not closely related to angiosperms, even if their true phylogenetic affinities remain opaque ... " (page 321, Discussion, Fertilization in Welwitschia, Ephedra, and Gnetum, Friedman 2015).

This begs the question, what was the mode of reproductive development and fertilization in gnetalean seed plants of the Permo-carboniferous (Z.-Q. Wang 2004), including the MRCA, which was postulated in Figure 3A representing one result of Sarah Mathews concatenated DNA analyses (page 231, 2009)?

The specific seed plant molecular phylogeny just cited places angiosperms basal to Permo-carboniferous cycads, ginkgos, cypresses, gnetaleans, and certain conifers, which when taking into account solid paleobotanical evidence positing at least a Permian origin for certain species of Coniferophyta, Cycadophyta, Ginkgophyta, and Gnetophyta, places original populations of stem group flowering plants and the MRCA solidly in the late Paleozoic.

Welwitschias are sister to extant Gnetum. Elegant molecular-phylogenetic studies on the evolutionary history of Gnetum from the Rydin Lab (Chen Hou et al. 2015) clearly support the sister relationship of Ephedra to Welwitschia and Gnetum, positing a Cretaceous origin of the latter genus.

Hou, Chen, A. M. Humphreys, O. Thureborn, and C. Rydin. 2015. New insights into the evolutionary history of Gnetum (Gnetales). Taxon 64(2): 239-253.

Node F5 in Figure 2 on page 245 of Chen Hou et al. (2015) is calibrated with the fossilized nearest relative of extant welwitschias, Cratonia cotyledon from the Lower Cretaceous Crato Formation (Rydin et al. 2003).

"... stem relatives of Gnetum were clearly present in the Early Cretaceous, and our topological and temporal results indicate that early lineage diversification in the crown group occurred in the Late Cretaceous, possibly as a consequence of the break-up of Gondwana ... " (Concluding remarks, page 249, Chen Hou et al. 2015).

At least one of the seed plant phytochrome protein amino acid sequence phylograms (Figure 4B on page 233, Mathews 2009) also places angiosperms basal to cycads, which are well-represented in the rock record of the Permian Period, and to certain other gymnosperms including gnetophytes.

"Based on fossil evidence and molecular clock calibration, the divergence between gymnosperms and angiosperms could be dated to about 300–350 million years ago (MYA) ... " (Abstract, X.-Q. Wang and J-H. Ran 2014).

References:

Bolinder, K., K. J. Niklas, and C. Rydin. 2015. Aerodynamics and pollen ultrastructure in Ephedra. American Journal of Botany 102(3): 457-470.

Friedman, W. E. and S. K. Floyd. 2001. The origin of flowering plants and their respective biology: a tale of two phylogenies. Evolution 55: 217-231.

Krassilov, V. A. 1977. The origin of angiosperms. Botanical Review 43(1): 143-176.

Krassilov, V. A. 1986. New floral structure from the Lower Cretaceous of Lake Baikal area. Review of Palaeobotany and Palynology 47: 9-16.

Krassilov, V. A. 1991. The origin of angiosperms: new and old problems. Trends in Ecology and Evolution 6(7): 215-220.

Krassilov, V. A. 1997. Angiosperm Origins: Morphological and Ecological Aspects. Sofia: Pensoft, 270 pp.

Krassilov, V. A. 2002. Character parallelism and reticulation in the origin of angiosperms. Chapter 29, Pp. 373-382 In: M. Syvanen and C. I. Kado (eds.), Horizontal Gene Transfer, San Diego: Academic Press, 445 pp.

Krassilov, V. A. 2009. Diversity of Mesozoic gnetophytes and the first angiosperms, Paleontological Journal 43(10): 1272-1280.

Krassilov, V. A. and S. R. Ash. 1988. On Dinophyton - protognetalean Mesozoic plant. Palaeontographica Abt. B 208: 33-38.

Krassilov, V. A. and E. V. Bugdaeva. 2000. Gnetophyte assemblage from the early Cretaceous of Transbaikalia. Palaeontographica Abt. B 253: 139-151.

Mathews, S. 2009. Phylogenetic relationships among seed plants: persistent questions? American Journal of Botany 96(1): 228-236.

Niklas, K. J. 2015. A biophysical perspective on the pollination biology of Ephedra nevadensis and E. trifurca. The Botanical Review 81(1): 28-41.

Rydin, C., B. A. Mohr, and E. M. Friis. 2003. Cratonia cotyledon gen. et sp. nov.: a unique Cretaceous seedling related to Welwitschia. Proceedings of the Royal Society of London, Series B, Biological Letters 270: 29-32.

Wang, X.-Q. and J-H. Ran. 2014. Evolution and biogeography of gymnosperms. Molecular Phylogenetics and Evolution 75: 24-40.

Wang, Z.-Q. 2004. A new Permian gnetalean cone as fossil evidence for supporting current molecular phylogeny. Annals of Botany 94: 281-288.

Notes added after-the-fact. Discussion of seed plant phylogeny on page 246 of Chen Hou et al. (2015), including deep Permo-carboniferous divergences of Coniferophyta, Cycadophyta, Ginkgophyta, and Gnetophyta (angiosperms are conveniently left-off the dated tree in Figure 2 on page 245) might be important to read in connection with the Mathews (2009) and X.-Q. Wang and J-H. Ran (2014) molecular-phylogenetic analyses.

Students will find relevant discussion in Friedman (1996), Price (1996), Friedman and Carmichael (1996, 1998), S.-X. Guo et al. (2009), Rydin and Friis (2010), Bolinder et al. (2016), Ickert-Bond and Renner (2016), Rydin and Hoorn (2016), and Tekleva (2016).

Simply put, if flowering plants are the sister group of modern gymnosperms including Ephedra, Gnetum, and Welwitschia, then why not explain further the "difficult problem" (page 246, Chen Hou et al. 2015) posed by conflicting seed plant phylogenies before exploring Gondwanan biogeographic patterns seen in the Gnetum stem group?

Interestingly, a paleobotanical study by Mamay et al. (1988) once drew a close connection of Permian gigantopteroids with Gnetum. But if the node leading to Gnetum (F5 on Figure 2, page 245 of Chen Hou et al. 2015) estimates an early Cretaceous divergence with Welwitschia, how can Permian delnorteas have anything to do with the evolutionary history of Gnetum?

"In light of the inadequacy of factual material that might assist in identifying descendants of Delnortea ... Gnetum offers a welcome avenue for deductive comparisons. Concomitantly, Delnortea provides a source of certain of the physical attributes of Gnetum; the two oddities complement each other in a manner rarely observed between two taxa as distantly separated in geologic time" (Discussion, Gnetum-like aspects of Delnortea, pages 1429-1430, Mamay et al. 1988).

Should phylogenetic hypotheses refute the supposed affinities of Delnortea abbottiae with Auritifolia waggoneri or Supaia thinnfeldioides peltasperms (see discussion in Booi et al. 2009), pteridosperms, cycadophytes, or Gnetum, then what were the evolutionary offshoots (if any) of gigantopteroids?

Finally, students of Gnetum and its relatives should read Tekleva (2016), and Volume 55, Number 1, which is the 2016 issue of Grana devoted to pollen ecology and diversity in Gnetales.

Additional References:

Bolinder, K., A. M. Humphreys, J. Ehrlén, R. Alexandersson, S. M. Ickert-Bond, and C. Rydin. 2016. From near extinction to diversification by means of a shift in pollination mechanism in the gymnosperm relict Ephedra (Ephedraceae, Gnetales). Botanical Journal of the Linnean Society 180(4): 461–477.

Booi, M., I. M. Van Waveren, and J. H. A. Van Konijnenburg-Van Cittert. 2009. The Jambi gigantopterids and their place in gigantopterid classification. Botanical Journal of the Linnean Society 161: 302-325.

Friedman, W. E. 1996. Introduction to biology and evolution of the Gnetales. International Journal of Plant Sciences 157(6 Supplement): S1-S2.

Friedman, W. E. and J. S. Carmichael. 1996. Double fertilization in Gnetales: implications for understanding reproductive diversification among seed plants. International Journal of Plant Sciences 157(6 Supplement): S77-S94.

Friedman, W. E. and J. S. Carmichael. 1998. Heterochrony and developmental innovation: evolution of female gametophyte ontogeny in Gnetum, a highly apomorphic seed plant. Evolution 52: 1016-1030.

Guo, S.-X., J.-G. Sha, L.-Z. Bian, and Y.-L. Qiu. 2009. Male spike strobiles with Gnetum affinity from the early Cretaceous in western Liaoning, northeast China. Journal of Systematics and Evolution 47(2): 93-102.

Hou, Chen, A. M. Humphreys, O. Thureborn, and C. Rydin. 2015. New insights into the evolutionary history of Gnetum (Gnetales). Taxon 64(2): 239-253.

Ickert-Bond, S. M. and S. S. Renner. 2016. The Gnetales: recent insights on their morphology, reproductive biology, chromosome numbers, biogeography, and divergence times. Journal of Systematics and Evolution 54(1): 1-16.

Mamay, S. H., J. M. Miller, D. M. Rohr, and W. E. Stein, Jr. 1988. Foliar morphology and anatomy of the gigantopterid plant Delnortea abbottiae from the Lower Permian of West Texas.  American Journal of Botany 75(9): 1409-1433.

Price, R. A. 1996. Systematics of the Gnetales: a review of morphological and molecular evidence. International Journal of Plant Sciences 157(6 Supplement): S40-S49.

Rydin, C. and E. M. Friis. 2010. A new early Cretaceous relative of Gnetales: Siphononospermum simplex gen. et sp. nov. from the Yixian Formation of northeast China. BMC Evolutionary Biology 10: 183.

Rydin, C. and C. Hoorn. 2016. The Gnetales: past and present. Grana 55(1): 1-4.

Tekleva, M. 2016. Pollen morphology and ultrastructure of several Gnetum species: an electron microscopic study. Plant Systematics and Evolution. 302(3): 291–303.



Late Triassic (Carnian) "Cycadophyte" Foliar Organs and Naming Detached Taeniopteroid Fossils (January 2015):

Neues Jahrbuch für Geologie und Paläontologie reports a find by Christian Pott and Ahti Launis (2015) of detached foliar organs, possibly belonging to an unknown bennettitalean or cycadophyte, which are not unlike strongly petiolate taeniopteroid leaves described as Nilssoniopteris (Figures 16.91 and 16.92 on page 693, T. N. Taylor et al. 2009).

Pott, C. and A. Launis 2015. Taeniopteris novomundensis sp. nov. – "cycadophyte" foliage from the Carnian of Switzerland and Svalbard reconsidered: How to use Taeniopteris? Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen (Stuttgart) 275(1): 19–31.

"After considerable personal discussion with J. H. A. Van Konijnenburg-Van Cittert ... and G. Zijlstra ... in April 2014, we all came to the conclusion that the best and simplest option is to leave Taeniopteris as an illegitimate genus and not to conserve it at all ... even if the genus is illegitimate, the various species are validly published (if done according to the rules of that time) and can, therefore, be legitimate ... So we can continue to use Taeniopteris as a fossil genus for leaves of a certain type and venation, of which no cuticle is known. As soon as epidermal anatomy becomes available, the material can be transferred to e.g. Nilssoniopteris, Nilssonia etc., or, in the case of a fertile fern, to Danaeopsis" (page 25, Pott and Launis 2015).

Additional discussion of morphotaxa, including nomenclatural considerations of the International Code (ICBN) are discussed on page 304 of Booi et al. (2009), and by McNeill and Turland (2011) and McNeill et al. (2012).

Booi and coworkers discuss the critical importance of describing the anatomy of the epidermis, including the nature of the stomatal apparatus, whether haplocheilic or syndetocheilic, and cuticle (absent or present) when classifying detached taeniopteroid foliar organs. The advent of modern paleobiological, phylogenetic, and theoretical approaches necessitates more sophisticated study of detached and shed Permo-carboniferous and Permo-triassic gigantopteroid and taeniopteroid "leaves," in my opinion.

Understanding scaling relationships between co-occurring plant fragments deposited in single bedding planes and discerning the "fingerprints of developmental regulation" (quoted from page 723, Sanders et al. 2007) from study of leaf midribs and margins to complement an investigation of the internal anatomy from study of polished thin-sections of permineralized fossils, and x-ray synchrotron tomography (Stein and Boyer 2006, Sanders et al. 2007, Christianson and Jernstedt 2009, Niklas and Kutschera 2009, Chartier et al. 2014, Rahman and Selena Y. Smith 2014, Rothwell et al. 2014) are approaches and techniques necessary to obtain sources of new data.

I suggest that the morphologies of the shoots that shed these "leaves" (whether long- or short [spur]-shoots) should also be ascertained from Principal Components Analysis (PCA) of theoretical morphospace occupied by the shoot apical meristem (SAM), nested foliar organs (bracts, leaves, sporophylls, and/or tepals [with foliar-bases described]), and subtending megaphyll (abscission layer present or absent, and gross morphology, simple and petiolate [entire margined or lobed] or compound), and so forth.

References:

Booi, M., I. M. Van Waveren, and J. H. A. Van Konijnenburg-Van Cittert. 2009. The Jambi gigantopterids and their place in gigantopterid classification. Botanical Journal of the Linnean Society 161: 302-325.

Chartier, M., F. Jabbour, S. Gerber, P. Mitteroecker, H. Sauquet, M. von Balthazar, Y. Staedler, P. R. Crane, and J. Schönenberger. 2014. The floral morphospace - a modern comparative approach to study angiosperm evolution. New Phytologist 204: 841-853.

Christianson, M. L. and J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: a quantitative analysis of the disposition of axillary structures. American Journal of Botany 96(11): 1957-1966.

McNeill, J., F. R. Barrie, W. R. Buck, V. Demoulin, W. Greuter, W. Hawksworth, P. S. Herendeen, S. Knapp, K. Marhold, J. Prado, W. F. Prud'homme van Reine, G. F. Smith, J. H. Wiersema, and N. J. Turland. 2012. International Code of Nomenclature for Algae, Fungi, and Plants (Melbourne Code) Adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011, Regnum Vegetabile 154. Königstein: Koeltz, 240 pp.

McNeill, J. and N. J. Turland. 2011. Major changes to the International Code of Nomenclature-Melbourne July 2011. Taxon 60(5): 1495-1497.

Niklas, K. J. and U. Kutschera. 2009. The evolutionary development of plant body plans. Functional Plant Biology 36: 682-695.

Rahman, I. A. and Selena Y. Smith. 2014. Virtual paleontology: computer-aided analysis of fossil form and function. Journal of Paleontology 88(4): 633-635.

Rothwell, G. W., S. E. Wyatt, and A. M. F. Tomescu. 2014. Plant evolution at the interface of paleontology and developmental biology: an organism-centered paradigm. American Journal of Botany 101(6): 899-913.

Sanders, H., G. W. Rothwell, and S. E. Wyatt. 2007. Paleontological context for the developmental mechanisms of evolution. International Journal of Plant Sciences 168: 719-728.

Stein, W. E. and J. S. Boyer. 2006. Evolution of land plant architecture: beyond the telomb theory. Paleobiology 32(3): 450-482.

Taylor, T. N., E. L. Taylor, and M. Krings. 2009. Paleobotany: The Biology and Evolution of Fossil Plants, Second Edition. Burlington: Elsevier Academic Press, 1230 pages.



Rudixylon (Petriellales) Provides Clues on the Paleophysiology of a Triassic Polar Forest Shrub (December 2014):

Chicago Journals published a significant find of stems and leaves of Rochipteris alexandriana and permineralized stems of Rudixylon serbetianum (Petriellales) from the Transantarctic Mountains, but the reproductive organs of the shrub-like nanophanerophytes that produced these shed vegetative axes are unknown.

Bomfleur, B., A-L. Decombeix, A. B. Schwendemann, I. H. Escapa, E. L. Taylor, T. N. Taylor, and S. McLoughlin. 2014. Habit and ecology of the Petriellales, an unusual group of seed plants from the Triassic of Gondwana. International Journal of Plant Sciences 175(9): 1062-1075.

Petriellales are a group of early Mesozoic gymnosperms with possible evolutionary ties to the Caytoniales (Figures 15.48 - 15.51, and pages 637-639, Chapter 15, Mesozoic Seed Ferns, T. N. Taylor et al. 2009). Fossils classified in this group of gymnosperms are scattered among more than 18 localities across southern Gondwana from South America to Australia. Seed pods described as Petriellaea triangulata might be homologous with angiosperm carpels but the gymnosperms that shed these organs are as yet unknown.

"... Many authors have noted the similarity of petriellalean cupules to those of the Caytoniales, a group of gymnosperms that continues to figure prominently in theories about the mysterious origin of flowering plants ... Recent hypotheses propose that the earliest angiosperms may have been small, woody shrubs that colonized disturbed sites in the damp understory of humid forests ... The reconstructed physiology and ecology of the Petriellales matches this life form to such detail that we suggest these unusual gymnosperms may represent convergent ecological analogues of early flowering plants" (page 1074, Discussion, Ecology and Paleoenvironment, Bomfleur et al. 2014).

Taking into account the morphology of reproductive short shoots of Winteraceae (i.e. the supposed source of shed Afropollis), Bomfleur and coauthors (op. cit.) should understand that petriellalean cupules are incompatible with tool kit models of floral development from spur shoot apical meristems.

"... We anticipate that the evident question-whether beyond the mere ecological similarity there may be phylogenetic relationships linking Petriellales with angiosperms-will be answered once more detailed information about their reproductive biology becomes available" (page 1074, Discussion, Ecology and Paleoenvironment, Bomfleur et al. 2014).

Confounding floral morphospace. Are certain homologies of reproductive organs of Caytonia proposed by J. A Doyle (pages 380-385, 1978), congruent with classical studies of Arber and Parkin, Leppik, Stebbins, and Takhtajan? No, when biochemical and evolutionary-developmental (evo-devo) models of cone and floral organization posited by Baum and Hileman (2006), Melzer et al. (2010), and Theißen and Melzer (2007) are considered.

Angiosperms are sister to conifers, cycads, ginkgophytes, and gnetophytes in several molecular phylogenetic analyses of seed plants, and fossil pollen studies (op. cit.) point to several possible Triassic flowering plant populations. Further, the reproductive male and female spur shoots of "living fossil" ginkgos are homologous with angiosperm flowers (Christianson and Jernstedt 2009).

Classical papers by Arber and Parkin (1907), Leppik (1960, 1968), and Stebbins (1951), among others, should be read together with these selections.

Arber, E. A. N. and J. Parkin. 1907. On the origin of angiosperms. Botanical Journal of the Linnaean Society 38: 28-80.

Baum, D. A. and L. C. Hileman. 2006. A developmental genetic model for the origin of the flower. Pp. 3-27 In: C. Ainsworth (ed.), Volume 20, Annual Plant Reviews, Flowering and Its Manipulation. Sheffield: Blackwell, 304 pp.

Chartier, M., F. Jabbour, S. Gerber, P. Mitteroecker, H. Sauquet, M. von Balthazar, Y. Staedler, P. R. Crane, and J. Schönenberger. 2014. The floral morphospace - a modern comparative approach to study angiosperm evolution. New Phytologist 204: 841-853.

Christianson, M. L. and J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: a quantitative analysis of the disposition of axillary structures. American Journal of Botany 96(11): 1957-1966.

Doyle, J. A. 1978. Origin of Angiosperms. Annual Review of Ecology and Systematics 9: 365-392.

Leppik, E. E. 1960. Early evolution of flower types. Lloydia 23(3): 72-92.

Leppik, E. E. 1968. Directional trend of floral evolution. Acta Biotheoretica 18A(1-4): 87-102.

Melzer, R., Y.-Q. Wang, and G. Theißen. 2010. The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower. Seminars in Cell & Developmental Biology 21(1): 118-128.

Rothwell, G. W., S. E. Wyatt, and A. M. F. Tomescu. 2014. Plant evolution at the interface of paleontology and developmental biology: an organism-centered paradigm. American Journal of Botany 101(6): 899-913.

Sayou, C., M. Monniaux, M. H. Nanao, E. Moyroud, S. F. Brockington, E. Thévenon, H. Chahtane, N. Warthmann, M. Melkonian, Y. Zhang, G. K.-S. Wong, D. Weigel, F. Parcy, and R. Dumas. 2014. A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science 343(6171): 645-648.

Stebbins, G. L. 1951. Natural selection and the differentiation of angiosperm families. Evolution 5: 299-324.

Theißen, G. and R. Melzer. 2007. Molecular mechanisms underlying origin and diversification of the angiosperm flower. Annals of Botany 100(3): 1-17.

I thank Rudolf Schmid, Ph.D. for bringing to my attention little known and often overlooked pioneering work by Leppik, among others. The extensive Schmid library, including books, card index, and reprints, is now housed at the New York Botanical Garden.

Despite considerable discussion in the literature on angiosperm phylogeny and evolution by J. A. Doyle and Frohlich, among others, Caytoniales and Petriellales probably had nothing to do with the "mysterious origin of flowering plants."

Notes added after-the-fact. Yet another dataset gleaned from fossilized leaves (foliar area and stomatal anatomy) unearthed from the Cretaceous Aptian to Albian Potomac Group and Albian Dakota Formation was deciphered by a mathematical model employed in several simulations using to infer the paleophysiology of the "earliest angiosperms" including so-called "breakout" taxa of crown group magnoliids and ANA-grade basal flowering plants (Lee et al. 2015).

Lee, A. P., G. Upchurch, Jr., E. H. Murchie, and B. H. Lomax. 2015. Leaf energy balance modelling as a tool to infer habitat preference in early angiosperms. Proceedings of the Royal Society of London, Series B, Biological Sciences 282: 20143052.

In view of Hochuli and Feist-Burkhardt's discovery of Afropollis (magnoliid pollen shed from possible Winteraceae), and angiosperm-like pollen from arid, boreal, and tropical paleoenvironments of Anisian time (2013), it is probably difficult to study the paleophysiology of stem group angiosperms based on studies of Cretaceous leaf fossils and modelling flowering plant population-paleoecologies in hypercapnic Lower Cretaceous environments.

Simply put, the habitat of ancient flowering plant populations was probably neither "dark and disturbed" or "wet and wild," which are persistent views held by certain students of Lower Cretaceous aquatic and terrestrial paleoecologies.



Long Branches of Unknown Angiosperm Stem Taxa May Affect Resolution of ANA Grade Species (November 2014):

Oxford Journals publishes yet another molecular phylogenetic study on the placement of Amborella trichopoda in relation to other ANA grade flowering plants.

Xi, Zhenxiang, L. Liang, J. S. Rest, and C. C. Davis. 2014. Coalescent versus concatenation methods and the placement of Amborella as sister to water lilies. Systematic Biology 63(6): 919-932.

The genome-scale molecular phylogenetic analyses by Zhenxiang Xi et al. (2014) are the first to resolve an Amborella + Nuphar phylogenetic couplet as sister to all other extant angiosperms when coalescent techniques are employed in computation, simulations, and tree-thinking.

"... Our results lend further empirical support for analyzing genome-scale data to resolve deep phylogenetic relationships using coalescent methods, and provide the most convincing evidence to date that Amborella plus Nymphaeales together represent the earliest diverging lineage of extant angiosperms" (page 929, Results and Discussion, Accommodating Elevated Rates of Substitution in Coalescent versus Concatenation Analyses, Xi et al. 2014).

Notes added after-the-fact. Related papers by Drew et al. (2014), D. W. Taylor and Gee (2014), Goremykin et al. (2015), Simmons and Gatesy (2015), and M. L. Taylor et al. (2015) should be read, among others. Further, the elaborate analyses published by Goremykin et al. (2015), yield results concordant with Xi et al. (2014), which are discussed above.

Relying on Felsenstein's premises and principles of phylogenetics, Simmons and Gatesy (2015) challenge the quoted passage above, which was published by Zhenxiang Xi et al. (2014). Certain phylogeneticists overuse terms such as "falsify," "rigor," and "sophisticated" to cast doubt on methodological details. Yet, long-branch attraction (LBA), reticulations introduced by allopolyploidy and horizontal transfer (HT), and paleobiological considerations (calibration of molecular phylogenies with fossils), might also lead to artifacts in cladograms possibly clouding or falsifying conclusions or inference.

Drew, B. T., B. R. Ruhfel, Stephen A. Smith, M. J. Moore, B. G. Briggs, M. A. Gitzendanner, P. S. Soltis, and D. E. Soltis. 2014. Another look at the root of the angiosperms reveals a familiar tale. Systematic Biology 63(3): 368-382.

Goremykin, V. V., S. V. Nikiforova, D. Cavalieri, M. Pindo, and P. Lockhart. 2015. The root of flowering plants and total evidence. Systematic Biology 64(5): 875-891.

Simmons, M. P. and J. Gatesy. 2015. Coalescence vs. concatenation: sophisticated analyses vs. first principles applied to rooting of the angiosperms. Molecular Phylogenetics and Evolution 91: 98-122.

Taylor, D. W. and C. T. Gee. 2014. Phylogenetic analysis of fossil water lilies based on leaf architecture and vegetative characters: testing phylogenetic hypotheses from molecular studies. Bulletin of the Peabody Museum of Natural History 55(2): 89-110.

Taylor, M. L., R. L. Cooper, E. L. Schneider, and J. M. Osborn. 2015. Pollen structure and development in Nymphaeales: insights into character evolution in an ancient angiosperm lineage. American Journal of Botany 102(10): 1685-1702.

"... regardless of whether Amborella alone is the sister to all other extant angiosperms or whether Amborella + Nymphaeales form a clade, one cannot infer the habit or habitat of the first angiosperms based on the morphology of extant taxa" (page 379, Discussion, Drew et al. 2014).

A study from the Friedman Lab (Povilus et al. 2015) reports on the reproductive biology of the IUCN Red List ANA-grade flowering plant Nymphaea thermarum, which is proposed as a new model angiosperm for future evo-devo and genomic research necessary for improving phylogenetic inference. Molecular-phylogenetic studies by the Sauquet Lab on magnoliids as a whole (Massoni et al. 2014, 2015) should also be read.

In 2015, The Guardian reported on a preliminary field study of undescribed water lilies from the Gibb River Region on the continent of Australia. The Australian Broadcasting Company presented another popular account of this spectacular discovery from The Kimberley Outback.

According to Bruce Cornet there is paleontological evidence of a water lily population represented by impressions in rocks of the Whitmore Point Member of the Moenave Formation (Lower Jurassic), southwestern North America. Paleobotanical data are needed to substantiate Cornet's anecdotal account.

Massoni, J., J. A. Doyle, and H. Sauquet. 2015. Fossil calibration of Magnoliidae, an ancient lineage of angiosperms. Palaeontologica Electronica 18.1.2FC.

Massoni, J., F. Forest, and H. Sauquet. 2014. Increased sampling of both genes and taxa improves resolution of phylogenetic relationships within Magnoliidae, a large and early-diverging clade of angiosperms. Molecular Phylogenetics and Evolution 70: 84-93.

Povilus, R. A., J. M. Losada, and W. E. Friedman. 2015. Floral biology and ovule and seed ontogeny of Nymphaea thermarum, a water lily at the brink of extinction with potential as a model system for basal angiosperms. Annals of Botany (Oxford) 115(2): 211-226.

Floating leaves and flowers of Nymphaea odorata var. rosea (Nymphaeaceae, Nymphaeales, Nymphaeanae) are pictured above. In 1978, I photographed these water lilies from ponds at the Butchart Gardens, Vancouver Island, northwestern North America, with Kodachrome ASA 25 film, and digitally-restored the two images for posting here.



Annals of Botany Publishes Special Issue on Cone and Floral Development (November 2014):

Issue 7 of Volume 114 of the Annals of Botany reports on current trends and future directions in the fast-moving biochemical- and plant-biological literature on flower development. Charlie Scutt and Michiel Vandenbussche (2014) discuss an "apparently abrupt Cretaceous origin" of flowering plants.

Students should read at least three papers of this special issue, and compare these evo-devo studies of the cone and floral tool kit with discussion of the Amborella trichopoda genome and paleopalynological studies.

Was a supposed Neocomian (mid-Hauterivian) origin of flowering plants (see page 282, 13.2.2, Data Collection and Analysis, Labandeira 2014) proposed by Friis et al. (2011), among others, an "abrupt" or somehow "sudden," saltational event in seed plant evolution?

Costanzo, E., C. Trehin, and M. Vandenbussche. 2014. The role of WOX genes in flower development. Annals of Botany (Oxford) 114 (7): 1545-1553.

Gramzow, L., L. Weilandt, and G. Theißen. 2014. MADS goes genomic in conifers: towards determining the ancestral set of MADS-box genes in seed plants. Annals of Botany (Oxford) 114(7): 1407-1429.

Melzer, R., A. Härter, F. Rümpler, S. Kim, P. S. Soltis, D. E. Soltis, and G. Theißen. 2014. DEF- and GLO-like proteins may have lost most of their interaction partners during angiosperm evolution. Annals of Botany (Oxford) 114 (7): 1431-1443.

"Our data suggest that the interactions governing flower development in core eudicots were already established at the base of extant angiosperms and remained highly conserved since then. Specifically, our results indicate that the heterodimerization between DEF-like and GLO-like proteins was already present in the [most common recent ancestor] MRCA of extant angiosperms and was virtually never rewired" (page 1438, Discussion, Conservation of the MADS-domain protein interaction pattern during angiosperm evolution, Melzer et al. 2014).

Based on a whole host of studies on gene regulatory network (GRN)-wiring in cone and floral development, is the canalized tool kit of the reproductive short- (spur-) shoot deeply-conserved from putative Permo-carboniferous seed plant populations of the MRCA?

"Darwin himself referred to the 'early origin and diversification of angiosperms' as 'an abominable mystery,' and the origin of the flower- and therefore flowering plants- is still a question ..."

The preceding statement is quoted from Page 86 of Pamela S. Soltis and Douglas E. Soltis (2014), Chapter 4. Flower diversity and angiosperm diversification. Pp. 85-102 In: J. L. Riechmann and F. Wellmer (eds.), Flower Development: Methods and Protocols, Volume 1110. New York: Springer, 475 pp.



Paleoherbivory in a Lower Permian (Kungurian) Riparian Florule of Southwestern North America (October 2014):

A significant study published by Chicago Journals of more than 2,000 rock samples from red beds of the Cisuralian Clear Fork Group (Kungurian [American Wolfcampian]) reveals arthropod and vascular plant interactions in a riparian paleoenvironment, including fossil evidence of boring, chewing, galling, ovipositioning, piercing, seed predation, sucking, and tissue consumption in gigantopteroids and peltaspermaleans.

Schachat, S. R., C. C. Labandeira, J. Gordon, D. Chaney, S. Levi, M. N. Halthore, and J. Alvarez. 2014. Plant-insect interactions from early Permian (Kungurian) Colwell Creek Pond, north-central Texas: the early spread of herbivory in riparian environments. International Journal of Plant Sciences 175(8): 855-890.

The study site is yet another place and geologic interval of Permian time where the gigantopteroid seed plant Evolsonia texana co-occurs with taeniopteroid foliage.

Platyspermic seeds, fragments of peltasperms (Auritifolia waggoneri and Supaia thinnfeldioides), and possible pteridosperms, sphenophytes, vojnovskyaleans (i.e. Sandrewia texana), and Walchia piniformis (Coniferophyta) were also found in bedding planes at Colwell with evolsonias.

Tropical, summer wet, terrestrial biomes of the early Permian Period contained innovative and unusual xeromorphic seed plant assemblages (DiMichele et al. 2004). The widely separated Delnortea and Evolsonia-dominated floras reported by Mamay et al. (1984), Mamay (1989), Ricardi et al. (1999), and Ricardi-Branco (2008) are examples of pervasive seed plant associations that might reflect long-term stasis in Permian terrestrial paleoenvironments.

Schachat and coworkers report two "overwhelmingly herbivorized taxa," Auritifolia waggoneri (Herbivory Index 3.08) and Taeniopteris sp. (Herbivory Index 1.36). Interestingly, "conspicuousness" of certain foliage was suggested as a cue for selective paleoherbivory in these plants (Abstract, Schachat et al. 2014), but Evolsonia texana (Herbivory Index 0.95) in these same bedding planes was evidently subjected to less predation than the other two species (Table 1 on page 858, Schachat et al. 2014).

This study begs at least two questions, among others. If detached herbivorized foliar organs provisionally classified as Taeniopteris sp. nov. were shed from short shoots subtended by Evolsonia texana leaves, were not lateral spur shoots of the gigantopteroid seed plant the conspicuous organ being eaten and potentially used by arthropods as habitat?

"Although we are considering Taeniopteris as a single species, it likely represents multiple species at Colwell Creek Pond [CCP]" (page 856, Geologic and Biologic Setting, The CCP Flora and Comparisons to Relevant Early Permian Floras, Schachat et al. 2014).

Instead of suggesting that one of the taeniopteroid morphotypes found in these red beds at Colwell Creek Pond [CCP] is Taeniopteris sp. nov. ["the probable cycadophyte" quoted from page 856] (Table 1 on page 858, Schachat et al. 2014) why not describe the anatomy of the leaf epidermis and ascertain whether or not taeniopteroid "leaves" were shed from a whole mother plant (this might be an undescribed gigantopteroid seed plant species with dimorphic foliage on long- and short shoots, respectively, or alternatively two separate sympatric species), and follow current recommendations in the International Code of Nomenclature (Melbourne Code), as agreed on by the paleobotanical community?

It was probably not the intent of Schachat and colleagues to explore paleobotanical problems of the Clear Fork red beds, which are probably underestimated or misunderstood by Chaney and DiMichele, among others. Rather, Schachat et al. (2014) are the first to document patterns and trends in gigantopteroid and peltaspermalean paleoherbivory, to suggest potential chemical and mechanical defenses of Permian seed plants against insect attack, and to tie their study of the Clear Fork Group red beds with similar studies at Elmo and Taint.

What alternative seed plant shoot configurations are possible in theoretical morphospace, based on taphonomic observations and frequency distribution of detached and shed foliar organs observed in discreet bedding planes from the numerous Lower Permian localities where Evolsonia texana and Taeniopteris co-occur?

Are two morphologically different but sympatric species found in these beds, or does the dimorphic foliage preserved in these rocks belong to an undescribed Permian gigantopteroid seed plant, which is neither a Auritifolia waggoneri or Supaia thinnfeldioides peltasperm, gnetophyte, pteridosperm, or taeniopteroid cycadophyte?

Anatomical studies of leaf bases such as the presence or absence of abscission layers and clasping or not, plus calculations of phyllotaxis, and scaling computation from bedding plane leaf frequencies of detached and shed foliar organs, and leaf morphometrics from in situ rock slab analyses, would be useful. Slab level studies on fossiliferous exposures of the North American Clear Fork Group of Cisuralian rocks are feasible.

Profusely illustrated herbivorized taeniopteroid foliar organs in Schachat et al. (2014) should be compared with Lonesomia mexicana, a gigantopteroid with Taeniopteris multinervis-type venation thought to be related to Delnortea abbottiae (Plate 3 on page 232, Weber 1997), and with discussion of Weber's lonesomias in a study of the Jambi gigantopterids by Booi et al. (2009). Taeniopteroid leaves of the T. multinervis-type were also found together with Delnortea abbottiae in South American Artinskian rocks by Ricardi et al. (1998), and from several North American Cisuralian (Leonardian and Wordian) rock exposures, including a report by the writer in coauthored published work (Mamay et al. 1984).

Multiple co-occurrences of taeniopteroid foliar organs with gigantopteroid megaphylls in Lower Permian (Artinskian and Cisuralian) rocks (more than 12 surface exposures on two different continents, and in core samples pulled-up from three exploratory bore-holes [some samples were recovered from layers buried several hundred meters deep in the wells]) cannot be dismissed as statistically and taphonomically insignificant but invite further investigation, in my opinion.

Further, there are "fingerprints of developmental regulation" seen in co-occurring gigantopteroid and taeniopteroid foliage, specifically in details of mid-rib anatomy and leaf-margin sculpting, offering clues not addressed in earlier work.

Background Reading:

Beck, A. L. and C. C. Labandeira. 1998. Early Permian folivory on a gigantopterid-dominated riparian flora from North central Texas. Palaeogeography, Palaeoclimatology, Palaeoecology 142: 139-173.

Booi, M., I. M. Van Waveren, and J. H. A. Van Konijnenburg-Van Cittert. 2009. The Jambi gigantopterids and their place in gigantopterid classification. Botanical Journal of the Linnean Society 161: 302-325.

DiMichele, W. A., A. K. Behrensmeyer, T. D. Olszewski, C. C. Labandeira, J. M. Pandolfi, S. L. Wing, and R. Bobe. 2004. Long-term stasis in ecological assemblages: evidence from the fossil record. Annual Review of Ecology, Evolution, and Systematics 35: 285-322.

DiMichele, W. A., D. S. Chaney, W. J. Nelson, S. G. Lucas, C. V. Looy, K. Quick, and W. Jun. 2007. A low diversity, seasonal tropical landscape dominated by conifers and peltasperms: early Permian Abo Formation, New Mexico. Review of Palaeobotany and Palynology 145(3-4): 249-273.

DiMichele, W. A. and R. A. Gastaldo. 2008. Plant paleoecology in deep time. Annals of the Missouri Botanical Garden 95: 144-198.

DiMichele, W. A. and R. W. Hook. 1992. 5. Paleozoic terrestrial ecosystems. Pp. 205--325 In: A. K. Behrensmeyer, J. D. Damuth, W. A. DiMichele, R. Potts, H.-D. Sues, and S. L. Wing (eds.), Terrestrial Ecosystems through Time, Evolutionary Paleoecology of Terrestrial Plants and Animals. Chicago: University of Chicago Press.

DiMichele, W. A., C. V. Looy, and D. S. Chaney. 2011. A new genus of gigantopterid from the middle Permian of the United States and China and its relevance to the gigantopterid concept. International Journal of Plant Sciences 172(1): 107-119.

Labandeira, C. C. and E. G. Allen. 2007. Minimal insect herbivory for the Lower Permian coprolite bone bed site of north-central Texas, USA, and comparison to other late Paleozoic floras. Palaeogeography, Palaeoclimatology, and Palaeoecology 247(3-4): 197-219.

Labandeira, C. C. and T. L. Phillips. 1996. A Carboniferous insect gall: insight into early ecologic history of the Holometabola. Proceedings of the National Academy of Sciences 93: 8470-8474.

Mamay, S. H. 1989. Evolsonia, a new genus of Gigantopteridaceae from the Lower Permian Vale Formation, North-central Texas.  American Journal of Botany 76(9): 1299-1311.

Mamay, S. H., J. M. Miller, and D. M. Rohr. 1984. Late Leonardian plants from West Texas: the youngest Paleozoic plant megafossils in North America. Science 223: 279-281.

Mamay, S. H., J. M. Miller, D. M. Rohr, and W. E. Stein, Jr. 1988. Foliar morphology and anatomy of the gigantopterid plant Delnortea abbottiae from the Lower Permian of West Texas.  American Journal of Botany 75(9): 1409-1433.

Ricardi, F., O. Rösler, and O. Odreman. 1999. Delnortea taphoflora (Gigantopteridaceae) of Loma de San Juan (Palmarito Formation, NW of Venezuela) and its palaeophytogeographical relationships in the Artinskian (Neopaleozoic).  Plantula 2(1-2): 73-86.

Ricardi-Branco, F. 2008. Venezuelan paleoflora of the Pennsylvanian-early Permian: paleobiogeographical relationships to central and western equatorial Pangaea. Gondwana Research 14(3): 297-305.

Weber, R. 1997. How old is the Triassic flora of Sonora and Tamaulipas, and news on Leonardian floras in Puebla and Hidalgo, Mexico. Revista Mexicana de Ciencias Geológicas 14(2): 225-243.

Notes added after-the-fact. Yet another paleoentomological paper by Schachat et al. (2015) should be read together with paleobiological studies at Colwell Creek Pond and Taint. This study details herbivorized remains of several morphotypes of detached taeniopteroid foliage preserved in freshwater Cisuralian pond deposits at Mitchell Creek Flats. Associated "gigantopterids" were Cathaysiopteris yochelsonii and Zeilleropteris wattii, which were gigantopteroids probably unrelated to Auritifolia waggoneri or Supaia thinnfeldioides peltasperms.

Several forms of Taeniopteris sp. in the paleolacustrine beds at Mitchell Creek Flats are morphospecies according to Schachat et al. (2015). Some of the leaf morphotypes found in the red beds at Colwell Creek Pond and Mitchell Creek Flats are considered detached foliar remains and seeds of cycadophytes possibly including Phasmatocycas.

Where are anatomical, morphometric, and scaling data to support these hypotheses?

Are ovules on some of the taeniopteroid leaves cycad-like or referable to the reproductive structures of Phasmatocycas?

Yet, there is another possible but unexplored interpretation to be proposed that opens windows to greater morphological, paleobiological, and taphonomic precision. Namely, that some of the taeniopteroid foliage preserved with gigantopteroid leaves in specific sedimentary layers could have been shed from Ginkgo-like short- [spur-] shoots subtended by Cathaysiopteris or Zeilleropteris megaphylls of long-shoots of a completely new kind of seed plant.

"Damage Type [DT] 143, a distinctive type of margin feeding with continuous, adjacent excisions occurs at Mitchell Creek Flats [MCF] on Taeniopteris spp. [Figs. 2.6-2.8] and on the gigantopterid Zeilleropteris spp. [Figs. 5.1-5.2] ..." (4.3.1.4 Remarks on page 836 of Schachat et al. 2015).

Do some herbivorized taeniopteroid organs preserved in rock layers at Colwell Creek Pond, Mitchell Creek Flats, and Taint belong to short-shoots of at least three species and genera of gigantopteroid seed plants, which are neither Auritifolia waggoneri or Supaia thinnfeldioides peltasperms, or gnetophytes, pteridosperms, and cycadophytes?

"This distribution of insect-mediated damage suggests a diverse community of opportunistic, generalized and specialized insect herbivores, including a guild of xeric-adapted gallers, engaged in a variety of feeding styles that overwhelmingly targeted Taeniopteris spp. as a host plant ..." (Abstract of Schachat et al. 2015).

Implications on the paleobiology of host mother plants at Colwell Creek Pond, Mitchell Creek Flats (MCF), and Taint, including herbivorized reproductive long- and short- [spur] shoots bearing dimorphic gigantopteroid and taeniopteroid foliar types, are profound. Yet, these authors at the United States National Museum (and its senior in-house paleobotanist) miss a golden opportunity to decipher, and to reconstruct alternative plant morphologies, which are critical in understanding the paleobiology of compact fertile short- [spur]- shoots or unrelated but herbivorized whole plants as insect habitat.

"Moreover, Taeniopteris spp. accounts for 56.9% of all [insect herbivore] interactions at MCF, an additional indication that it was the most intensely herbivorized taxon. Taeniopteris spp. was also the only plant host consumed by the four major broadleaf feeding guilds ..." (6. Conclusions 3. Opportunistic host-seeking behavior by insect herbivores on page 845 of Schachat et al. 2015).

Paleoecologies of intensely herbivorized taeniopteroid foliar material might be better understood when the morphology of the shoots that shed these leaf-like organs is deduced.

Schachat, S. R., C. C. Labandeira, and D. S. Chaney. 2015. Insect herbivory from early Permian Mitchell Creek Flats of north-central Texas: opportunism in a balanced component community. Palaeogeography, Palaeoclimatology, and Palaeoecology 440(3-4): 830-847.

The image above is a 280 million year old calcitic and limonitic permineralization of the midrib of the abaxial leaf surface of Delnortea abbottiae (USNM 372427) with possible preserved tissue damage or uneven weathering (actual size). The tiny pits on the midrib of the leaf may be bite marks or traces of ovipositioning.

Do certain taeniopteroid remains in Artinskian and Cisuralian Delnortea beds also belong to reproductive short-shoots of a gigantopteroid seed plant, which is not assignable to Peltaspermales, Gnetales, or Cycadales?



High DNA Content, Karyology, and Unusual Microsporogenesis in ANA grade Hydatellaceae (September 2014):

The Botanical Society of America publishes significant findings from the Rudall Lab on the chromosome biology of Trithuria submersa (Hydatellaceae, Nymphaeales, Nymphaeanae), revealing water lily-like nuclear DNA content. Unusual microsporogenesis, a chromosome number of 2n = 56, and allopolyploidy is revealed in a study of a monocot-like, aquatic ANA-grade basal angiosperm.

"The meiotic peculiarities of simultaneous cytokinesis with traces of a successive character observed in T. submersa could be regarded as representative of the evolutionary 'experimentation' that occurred in early angiosperms before fixation of the more typical and canalized types of microspore development that characterize most flowering plants ..." (page 1453, Results and Discussion, Kynast et al. 2014).

Kynast, R. G., J. A. Joseph, J. Pellicer, M. M. Ramsay, and P. J. Rudall. 2014. Chromosome behavior at the base of the angiosperm radiation: Karyology of Trithuria submersa (Hydatellaceae, Nymphaeales). American Journal of Botany 101(9): 1447-1455.

Related papers by Friedman et al. (2012) and Iles et al. (2014) should be read, among others.

Friedman, W. E., J. B. Bachelier, and J. I. Hormaza. 2012. Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early-diverging flowering plants. American Journal of Botany 99(6): 1083–1095.

Iles, W. J. D., C. Lee, D. D. Sokoloff, M. V. Remizowa, S. R. Yadav, M. D. Barrett, R. L. Barrett, T. D. Macfarlane, P. J. Rudall, and Sean W. Graham. 2014. Reconstructing the age and historical biogeography of the ancient flowering-plant family Hydatellaceae (Nymphaeales). BMC Evolutionary Biology 14: 102.



Support for a Gnepine Hypothesis Builds, and Flowering Plants Are the Sister Group of Gymnosperms (June 2014):

Several reviews having bearing on the origin of flowering plants were published in the first quarter of 2014. Milestone reviews included papers written by Paul M. Barrett (2014), William L. Crepet (2014), James A. Doyle and Peter K. Endress (2014), Susana Magallón (2014), Xiao-Quan Wang and Jin-Hua Ran (2014), and Xin Wang (2014).

A detached megasporophyll of extant Cycas revoluta (Cycadaceae, Cycadales) is pictured to the left. The hairy megasporophyll bears a pair of bright-red ripened seeds and one brownish immature ovule on the lower edges of the dissected leaf.

Cycad embryos are protected by an indurate sarcotesta of the seed. Colorful seeds of Mesozoic cycads were browsed, partially digested, and dispersed by stegosaurians according to certain paleobiologists.

Two reviews written and published by J. A. Doyle and Endress (2014), and X.-Q. Wang and J-H. Ran (2014), respectively, offer contrasting views on angiosperms, gymnosperms, and divergence[s] from the most recent common ancestor (MRCA), but coevolution is not discussed.

Wang, X.-Q. and J-H. Ran. 2014. Evolution and biogeography of gymnosperms. Molecular Phylogenetics and Evolution 75: 24-40.

Doyle, J. A. and P. K. Endress. 2014. Integrating early Cretaceous fossils into the phylogeny of living angiosperms: ANITA lines and relatives of Chloranthaceae. International Journal of Plant Sciences 175(5): 555-600 (with supplements).

Angiosperms are basal to conifers, cycads, ginkgos, and gnetophytes in several phylogenetic analyses cited and debated in these two reviews. Fossil-calibrated trees discussed by Xiao-Quan Wang and Jin-Hua Ran (2014) posit a Permo-carboniferous or Permo-triassic origin of the flowering plant stem group. Another compilation pieces together evidence from Mesozoic fossils (James A. Doyle and Endress 2014) illuminating radiation of basal angiosperms.

"Based on fossil evidence and molecular clock calibration, the divergence between gymnosperms and angiosperms could be dated to about 300–350 million years ago (MYA) ... " (Abstract, X.-Q. Wang and J-H. Ran 2014).

James A. Doyle and Endress (2014) are skeptical of some findings in the physiologic literature, and are not enthusiastic of [some] molecular-phylogenetic studies that suggest a late Paleozoic split of gymnosperms from angiosperms:

"Our results challenge this scenario [that the terrestrial ANITA lines were xerophobic, Feild et al. 2004, 2009, and that rates of angiosperm diversification were initially low and did not speed up until origin of the mesangiosperm clade, Magallón and Sanderson 2001] by showing that the ANITA lines were radiating in the Aptian-Albian, alongside Chloranthaceae and extinct relatives, magnoliids, monocots, and primitive eudicots ... This could mean that angiosperm diversification in general was being inhibited by external environmental factors before the Cretaceous, rather than by ecophysiological limitations of the first angiosperms, or that angiosperms are not as old as molecular dating implies" (page 592, Results and Discussion: Implications for Pre-Cretaceous History of the Angiosperm Line, James A. Doyle and Endress 2014).

Susana Magallón offers insight from a review of Bayesian priors, calibrations, and artifacts due to long-branch attraction in the several competing seed plant molecular-phylogenetic analyses listed in Table 1 on pages 7, 8, and 9 (Magallón 2014), which are also discussed by X.-Q. Wang and J-H. Ran (2014).

" ... studies of angiosperms depend a lot on our knowledge of gymnosperms given the sister relationship between the two groups" (page 25, X.-Q. Wang and J-H. Ran 2014).

Magallón, S. 2014. A review of the effect of relaxed clock method, long branches, genes, and calibrations in the estimation of angiosperm age. Botanical Sciences (Boletín de la Sociedad Botánica de México) 92[1]: 1-22.

"These combined observations clearly indicate that the molecular data contain a signal congruent with an angiosperm age much older than the earliest angiosperm fossils. But I would like to argue that a very old angiosperm age is not the only possible interpretation of such molecular signal" (Discussion, page 16, Magallón 2014).

A fifth review was published early in 2014 by William L. Crepet.

Crepet, W. L. 2014. Advances in Flowering Plant Evolution. eLS (Citable Reviews in the Life Sciences [Fossils and Evolution]). Chichester: John Wiley & Sons, Ltd, 11 pp.

"What is surprising is the scale of the uncertainty surrounding our basic knowledge of angiosperms. Angiosperm relationships are only now being resolved through the application of various algorithms to the combination of molecular genetics-derived data and morphological data. Yet the relationship of the angiosperms themselves to nonangiospermous seed plants, or understanding the origin of this major group, still remains a hotly contested mystery ... " (Abstract, Crepet 2014).

The sixth and final compilation ties-in with Professor Crepet's eloquent review:

Wang, Xin. 2014. The megafossil record of early angiosperms in China since 1930s. Historical Biology: An International Journal of Paleobiology, DOI: 10.1080/08912963.2014.889695.

Notes added after-the-fact. A diffuse relationship between an explosive superradiation of flowering plants with frugivorous bats, multituberculates, ornithischians, passerines, primates, and rodents, is the subject of a paper published by Ove Eriksson (2016) in the Biological Reviews of the Cambridge Philosophical Society.

Eriksson, O. 2016. Evolution of angiosperm seed disperser mutualisms: the timing of origins and their consequences for coevolutionary interactions between angiosperms and frugivores. Biological Reviews 91(1): 168–186.

Fruits of Degeneria vitiensis open in a "butterfly" fashion exposing several bright orange or red seeds that dangle from the fruit casing by funiculi (right-hand image). Frugivorous fruit doves and parrots consume and disperse seeds of degenerias, which are endemic magnoliids of the Fiji archipelago (J. M. Miller 1989).

A coevolutionary origin and radiation of angiosperms and ornithischians has been proposed by several paleontologists. Paul Barrett revisits some of these ideas in his contribution to a 2014 volume of the Annual Review of Earth and Planetary Sciences:

"Although dinosaur herbivores lived through several major events in floral evolution, there is currently no evidence for plant-dinosaur coevolutionary interactions" (page 207, Abstract, Barrett 2014).

Background Reading:

Barrett, P. M. 2014. Paleobiology of herbivorous dinosaurs. Annual Review of Earth and Planetary Sciences 42: 207-230.

Eriksson, O. 2008. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence. International Journal of Plant Sciences 169(7): 863-870.

Friis, E. M., P. R. Crane, and K. R. Pedersen. 2011. Early Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press, 596 pp.

Miller, J. M. 1989. The archaic flowering plant family Degeneriaceae: its bearing on an old enigma. National Geographic Research 5(2): 218-231.

Morley, R. J. 2001. Why are there so many primitive angiosperms in the rain forests of Asia-Australasia. Pp. 185-200 In: I. Metcalfe, J. M. B. Smith, M. Morwood, and I. Davidson (eds.), Faunal and Floral Migrations and Evolution in SE Asia-Australasia. Lisse: Swets and Zeitlinger, 419 pp.

Tiffney, B. H. 1984. Seed size, dispersal syndromes, and the rise of the angiosperms: evidence and hypothesis. Annals of the Missouri Botanical Garden 71: 551-576.

Weishampel, D. B. and C.-M. Jianu. 2000. Chapter 5, Plant-eaters and ghost lineages: dinosaurian herbivory revisited. Pp. 123-143 In: H.-D. Sues (ed.), Evolution of Herbivory in Terrestrial Vertebrates: Perspectives from the Fossil Record. Cambridge: Cambridge University Press, 256 pp.

Based on the review by Weishampel and Jianu (2000) is Bakker's proposal quoted below, accurate or plausible?

"The most prevalent coevolutionary hypothesis proposed that changes in dinosaur browsing behavior fostered the origin and radiation of angiosperms [Bakker 1978]" (page 220, Plant-dinosaur Interactions: Coevolution or Coincidence? Barrett 2014).



Evolution of a LFY Protein Homeodomain Unfolds in Streptophytes, Bryophytes, and Seed Plants (February 2014):

The American Association for the Advancement of Science (AAAS) publishes another critically important study with broad implications on the evolution the DNA-binding homeodomain of modular tool kit transcription factors (TFs) at the heart of cone and floral development.

"A highly conserved and essential TF [LFY homeodomain protein] evolved radical shifts in DNA binding specificity by a mechanism that does not require gene duplication." (page 648, Sayou et al. 2014).

Sayou, C., M. Monniaux, M. H. Nanao, E. Moyroud, S. F. Brockington, E. Thévenon, H. Chahtane, N. Warthmann, M. Melkonian, Y. Zhang, G. K.-S. Wong, D. Weigel, F. Parcy, and R. Dumas. 2014. A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science 343(6171): 645-648.

Further, dimeric Leafy (LFY) protein and auxin form modules, which together with polarity networks (PINs) help determine floral primordia in SAMs of some model angiosperms.

"Its emergence [of a reproductive regulatory network] probably involved changes in cis-elements of recruited targets, to place them under LFY control, as well as the establishment of novel protein-protein interactions." (page 351, Moyroud et al. 2010).

Moyroud, E., E. Kusters, M. Monniaux, R. Koes, and F. Parcy. 2010. LEAFY blossoms. Trends in Plant Science 15: 346-352.

"Our study reveals that the LFY master regulator, which determines flower meristem fate and controls the expression of floral organ identity genes, shares structural similarity with other HTH proteins, indicating that this universal DNA-binding motif has also been adopted in plants to trigger major developmental switches."

The preceding paragraph is quoted from page 2635 of C. Hamès, D. Ptchelkine, C. Grimm, E. Thévenon, E. Moyroud, F. Gérard, J.-L. Martiel, R. Benlloch, F. Parcy, and C. W. Müller (2008), Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins. The EMBO Journal 27: 2628-2637.

The left-hand image is reproduced from Figure 6 on page 2634 of Hamès et al. (2008), "Comparison of LFY-C with paired and homeodomain DNA binding.

(A) Two orthogonal views of LFY-C helices α1 - α3 bound to their DNA target site [red] superimposed with the three helical bundle core of the N-terminal subdomain of the paired domain of Drosophila Prd [blue, PDB-id: 1pdn]. (B) Superposition with the homeodomain of Drosophila engrailed bound to DNA [yellow, PBD-id: 1hdd], where the centre of recognition helix α3 inserts into the major groove."

Reprinted by permission from Macmillan Publishers Ltd: The European Molecular Biology Organization (EMBO) Journal, Hamès, C., D. Ptchelkine, C. Grimm, E. Thevenon, E. Moyroud, F. Gérard, J.-L. Martiel, R. Benlloch, F. Parcy, and C. W. Müller. 2008. Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins, The EMBO Journal 27: 2628-2637, copyright ©2008.

Future research to decipher possible molecular coevolution of LFY and Engraled protein should take into account evolutionary theory on the origin and diversification of cis-regulatory modules (CRMs) and gene regulatory networks (GRNs) that orchestrate development of animal and plant organs and bodies.

Carroll, S. B. 2008. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134(1): 25-36.

Note added after-the-fact. "Provocative" findings by Sayou et al. (2014) generated further molecular-phylogenetic study, analysis, and comment by University of California, Berkeley researchers, inviting debate and discussion of LFY gene duplication and neofunctionalization, and evolution of a DNA-binding homeodomain in land plant lineages.

Brunkard, J. O., A. M. Runkel, and P. C. Zambryski. 2015. Comment on "A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity." Science 347(6222): 621.

Brockington, S. F., E. Moyroud, C. Sayou, M. Monniaux, M. H. Nanao, E. Thévenon, H. Chahtane, N. Warthmann, M. Melkonian, Y. Zhang, G. K-S. Wong, D. Weigel, R. Dumas, and F. Parcy. 2015. Response to Comment on "A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity." Science 347(6222): 621.



Stomatal Guard Cell Size as Proxy for Paleopolyploidy in Vascular Plants Including Angiosperms (January 2014):

Paleogenome size in land plants is estimated from morphometric studies of stomatal guard cell length in this milestone paper that has direct bearing on evolution of seed plants and the origin of angiosperms. Data suggest a relationship between paleopolyploidy, extinction of neopolyploids, adaptive radiations, and the paleoecology of pCO2.

"Both palaeopolyploidy events [350 MYA and 200 MYA, Jiao et al. 2011] appear to coincide with relatively high, yet declining, atmospheric carbon dioxide concentration (Fig. 2c, d). However, using the fossil record rather than molecular dating techniques, the earlier event actually corresponds with the initial radiation of seed plants in the Late Devonian and Mississippian, while the latter is contemporaneous with the Triassic–Jurassic boundary and hence significantly pre-dates the earliest morphologically recognisable angiosperms (see Bateman and Hilton 2006) ..." (Page 639 and 640, Lomax et al. 2014).

Lomax, B. H., J. Hilton, R. M. Bateman, G. R. Upchurch, J. A. Lake, I. J. Leitch, A. Cromwell, and C. A. Knight. 2014. Reconstructing relative genome size of vascular plants through geological time. New Phytologist 201(2): 636–644.

Two key paleobiological papers (McElwain and Punyasena 2007, Retallack 2009) provide additional overlooked commentary on the use of stomatal indices as proxies "for past CO2 spikes."

McElwain, J. C. and S. W. Punyasena. 2007. Mass extinction events and the plant fossil record. Trends in Ecology and Evolution 22(10): 548-557.

Retallack, G. J. 2009. Greenhouse crises of the past 300 million years. GSA Bulletin 121(9-10): 1441-1455.

For purposes of future morphological phylogenetic analyses of seed plants the stomatal characters listed in Table 1 by Rudall et al. (Pages 602-603, 2013) should be employed by students, and polarity arguments posed by these authors must be discussed.

Rudall, P. J., J. Hilton, and R. M. Bateman. 2013. Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants. New Phytologist 200(3): 598-614.

Notes added after-the-fact. Numerous studies that employ paleo-proxies, mathematical models of atmospheric carbon dioxide concentration, and paleo-physiology of seed plant hydraulic morphospaces have been published. Certain lines of paleobiological research might have a bearing on paleopolyploids ascertained from morphometric studies of stomatal guard cell length (see Lomax et al. 2014), and the origin angiosperms.

"Baileyan trends," are predicted by Feild and Brodribb (2013) but to identify these in ancient lineages such as Degeneriaceae + Himantandraceae (page 89, Figure 3, Massoni et al. 2014), will require more work.

To the right is a scanning electron micrograph (SEM) of the epidermis of a leaf-like staminode of Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnolianae). Epidermal cells and two guard cells surrounding a stomate are visible. The anatomy and development of the stomatal pore of Degeneria vitiensis is probably unstudied.

Staminodes of Degeneria vitiensis are covered with bright-yellow, oily exudate and emit volatile hydrocarbons (VOCs) including fragrant terpenes and acetate esters. Fragrance analyses and the ecological studies of pollination in both species of Degeneria are needed.

The scanning electron micrograph is from a dissected and fixed floral organ collected in a Degeneria tree canopy at Mount Naitaradamu, Fiji (J. M. Miller 1989).

What can the paleophysiology of seed plant conducting tissues and the fragrance-emitting stomatal pore (right-hand SEM) tell us about the evolution of magnoliids and coevolution with insect antagonists?

Possibly a great deal, but only if Angiosperm Phylogeny Group [APG] IV (2016) is accepted with a grain of salt and by embracing evolutionary development (evo-devo) as sources of morphological novelties in diverging seed plant lineages including angiosperms.

Consideration of allopolyploidy in deep-time (Jiao et al. 2011) as starting points of flowering plant lineage diversification could be pivotal. If the first angiosperms evolved from allopolyploid populations spread across thousands of kilometers then how can flowering plants be monophyletic?

Wilson and Knoll (page 344, 2010) state an important point in the introductory paragraph of the discussion on wood evolution and their analyses of hydraulic morphospaces:

"Molecular phylogenies suggest that angiosperms are sister to all other living seed plants."

Adoption of the ideas just stated would invalidate some proposals on the origin of angiosperms and their supposed paleoecologies stated by Boyce, Brodribb, J. A. Doyle, and Feild, among others.

Background Reading:

APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20.

Boyce, C. K. 2005. Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31(1): 117-140.

Boyce, C. K. and A. H. Knoll. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28(1): 70-100.

Boyce, C. K. and M. A. Zwieniecki. 2012. Leaf fossil record suggests limited influence of atmospheric CO2 on terrestrial productivity prior to angiosperm evolution. Proceedings of the National Academy of Sciences 109(26): 10403-10408.

Feild, T. S. 2005. Chapter 24. Are vessels in seed plants evolutionary innovations to similar ecological contexts? Pp. 501-516 In: N. M. Holbrook and M. A. Zwieniecki (eds.), Vascular Transport in Plants, New York: Academic Press, 564 pp.

Feild, T. S. and T. J. Brodribb. 2013. Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks. New Phytologist 199(3): 720-726.

Franks, P. J., D. L. Royer, D. J. Beerling, P. K. Vandewater, D. J. Cantrill, M. M. Barbour, and J. A. Barry. 2014. New constraints on atmospheric CO2 concentration for the Phanerozoic. Geophysical Research Letters 41: 4685-4694.

Jiao, Y., N. L. Wickett, S. Ayyampalayam, A. S. Chanderbali, L. Landherr, P. E. Ralph, L. P. Tomsho, Y. Hu, H. Liang, P. S. Soltis, D. E. Soltis, S. W. Clifton, S. E. Schlarbaum, S. C. Schuster, H. Ma, J. Leebens-Mack, and C. W. dePamphilis. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345): 97-100.

Massoni, J., F. Forest, and H. Sauquet. 2014. Increased sampling of both genes and taxa improves resolution of phylogenetic relationships within Magnoliidae, a large and early-diverging clade of angiosperms. Molecular Phylogenetics and Evolution 70: 84-93.

McElwain, J. C., I. Montañez, J. D. White, J. P. Wilson, and Y. Yiotis. 2016. Was atmospheric CO2 capped at 1000 ppm over the past 300 million years? Palaeogeography, Palaeoclimatology, and Palaeoecology 441(3-4): 653-658.

McElwain, J. C., K. J. Willis, and K. J. Niklas. 2011. 5. Long-term fluctuations in atmospheric CO2 concentration influence plant speciation rates. Pp. 122-140 In: T. R. Hodkinson, M. B. Jones, S. Waldren, and J. A. N. Parnell (eds.), Climate Change, Ecology and Systematics. Cambridge: Cambridge University Press, 524 pp.

Miller, J. M. 1989. The archaic flowering plant family Degeneriaceae: its bearing on an old enigma. National Geographic Research 5(2): 218-231.

Wilson, J. P. and A. H. Knoll. 2010. A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants. Paleobiology 36: 335-355.



Amborella Is American Association for the Advancement of Science (AAAS) Genome of the Year (December 2013):

Volume 342, Number 6165 of Science publishes three significant papers on paleopolyploidy and the genome ecology of Amborella trichopoda, which is a specialized, root-sprouting understory endemic shrub of the high island of New Caledonia (Nouvelle Caledonie), southwest Pacific Ocean.

"The Amborella genome is a pivotal reference for understanding genome and gene family evolution throughout angiosperm history. Genome structure and phylogenomic analyses indicate that the ancestral angiosperm was a polyploid with a large constellation of both novel and ancient genes that survived to play key roles in angiosperm biology" (Structured Abstract Discussion, Amborella Genome Project 2013).

Amborella Genome Project. 2013. The Amborella genome and the evolution of flowering plants. Science 342(6165): 1467.

"Transposable elements in Amborella are ancient and highly divergent, with no recent transposon radiations" (Abstract, Amborella Genome Project 2013).

Earlier installments of this ongoing work were published in Genome Biology by D. E. Soltis et al. (2008) and Zuccolo et al. (2011).

Detailed next-generation sequencing studies by Srikar Chamala et al. (2013) report use of fluorescence probes to disentangle and decipher the large genome of Amborella trichopoda (Amborellaceae), a nonmodel basal angiosperm.

Chamala, S., A. S. Chanderbali, J. P. Der, T. Lan, B. Walts, V. A. Albert, C. W. dePamphilis, J. Leebens-Mack, S. Rounsley, S. C. Schuster, R. A. Wing, N. Xiao, R. Moore, P. S. Soltis, D. E. Soltis, and W. B. Barbazuk. 2013. Assembly and validation of the genome of the nonmodel basal angiosperm Amborella. Science 342(6165): 1516-1517.

This issue of Science also contains a study on horizontal transfer (HT) of mitochondrial DNA in Amborella trichopoda.

Rice, D. W., A. J. Alverson, A. O. Richardson, G. J. Young, M. V. Sanchez-Puerta, J. Munzinger, K. Berry, J. L. Boore, Y. Zhang, C. W. dePamphilis, E. B. Knox, and J. D. Palmer. 2013. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342(6165): 1468-1473.

Research findings by the Palmer Lab on the mitochondrial genome of Liriodendron might be relevant.

Richardson, A. O., D. W. Rice, G. J. Young, A. J. Alverson, and J. D. Palmer. 2013. The "fossilized" mitochondrial genome of Liriodendron tulipifera: ancestral gene content and order, ancestral editing sites, and extraordinarily low mutation rate. BMC Biology 11: 29.

These workers adopt the curious phrase first coined by Zuccolo et al. (page 3, 2011), "throughout angiosperm history," and suggest an asymptotic age for the origin of the clade "≈200 MYA," which is the approximate date of the end-Triassic mass extinction. Yet, fossil calibration and statistical inference on origin(s) or divergence(s) of the angiosperm stem(s) awaits further genomic and tool kit studies (Bliss et al. 2013), and paleobotanical evidence of amborellas (Krassilov and Golovneva 2004) should be discussed.

Krassilov, V. A. and L. B. Golovneva. 2004. A minute mid-Cretaceous flower from Siberia and implications for the problem of basal angiosperms. Geodiversitas 26(1): 5-15.

Paleontologic data will be required to validate molecular phylogenies (Peterson et al. 2007).

"The interface of these three subject areas (Figure 1 on Page 778), molecular evolution, evolutionary developmental ('evo-devo') biology, and palaeoecology, is the theme of Molecular Palaeobiology, as it [the approach] uniquely integrates the patterns written in the two historical records, genomic and geological ... "

The preceding statement is from Page 777 of Kevin J. Peterson, R. E. Summons, and P. C. J. Donoghue (2007), Molecular Palaeobiology, Palaeontology 50(4): 775-804.

Paleohexaploidy i.e. the gamma (γ)- triplication at the heart of the radiation of eudicots (Jiao et al. 2012) is apparently absent in the evolutionary history of the New Caledonian endemic species Amborella trichopoda according to the studies cited above. This begs four (4) questions, among others:

Is the single paleopolyploid event discerned from study of the Amborella genome including an epsilon (ε)- whole genome duplication (WGD), which is depicted as the asterisk in the figured Structured Abstract of Amborella Genome Project (2013), part of the ancient alpha (α)- swarm of WGDs modeled by Jiao et al. (2011)?

If angiosperms in the broad sense are fundamentally paraphyletic (and/or polyphyletic), and WGDs (including the γ-triplication) are a result of classic allopolyploidy in paleopopulations of genetically unrelated evolutionary lines, how can a single ancestral Amborella genome be manifest "throughout angiosperm history" without genetic input from unrelated seed plant populations?

Should students of evo-devo recompute a combined morphological- and molecular phylogenetic analysis of flowering plants to reflect extreme conservation of the floral tool kit and to incorporate allopolyploidy at the base of the angiosperm stem(s)?

Since the reproductive branch bauplan of Caytonia is incongruent with most models of cone and floral evo-devo, should paleobotanists dispose of Caytoniales, which are basal to the flowering plant clade in several morphological- and combined morphological-molecular phylogenetic analyses of seed plants?

Students should read a review on the interplay of evo-devo and phylogenetics with the paleobiology of evolutionary scales and probabilities by David Jablonski (2000).

"Although the macroevolutionary exploration of developmental genetics has just begun, considerable progress has been made in understanding the origin of evolutionary novelty in terms of the potential for coordinated morphological change and the potential for imposing uneven probabilities on different evolutionary directions" (Jablonski 2000).

The preceding statement is quoted from the Abstract on Page 15 of David Jablonski (2000), Micro- and macroevolution: scale and hierarchy in evolutionary biology and paleobiology, Paleobiology 26(4): 15-52.

Further, angiosperms are sister to conifers, cycads, ginkgophytes, and gnetophytes in several molecular phylogenetic analyses of seed plants, and fossil pollen studies point to several possible Triassic flowering plant populations.

Based on solid morphological evidence the reproductive male and female spur shoots of "living fossil" ginkgos are homologous with angiosperm flowers (Christianson and Jernstedt 2009).

Christianson, M. L. and J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: a quantitative analysis of the disposition of axillary structures. American Journal of Botany 96(11): 1957-1966.

Ginkgo biloba is suggested as a prospective "model gymnosperm" on page 588 of Rachel Spicer and A. Groover (2010).

Posit morphological and molecular tool kit findings (Melzer et al. 2010) and the phylogenetics of phytochrome protein amino acid sequences (Figure 4B on page 233, Mathews 2009) and concatenated angiosperm and gymnosperm DNA data sets (see Figure 3A on page 231 and source data in the cited references, Mathews 2009), the Ancestral Angiosperm Genome Project team should adopt Ginkgo biloba as a "poster boy [or girl]."

Mathews, S. 2009. Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. American Journal of Botany 96(1): 228-236.

Melzer, R., Y.-Q. Wang, and G. Theißen. 2010. The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower. Seminars in Cell & Developmental Biology 21(1): 118-128.

Zuccolo, A., J. E. Bowers, J. C. Estill, Z. Xiong, M. Luo, A. Sebastian, J. L. Goicoechea, K. Collura, Y. Yu, A. Chanderbali, D. E. Soltis, S. Chamala, B. Barbazuk, P. S. Soltis, V. A. Albert, H. Ma, D. Mandoli, J. Banks, J. E. Carlson, J. Tompkins, C. W. dePamphilis, R. A. Wing, and J. Leebens-Mack. 2011. A physical map for the Amborella trichopoda genome sheds light on the evolution of angiosperm genome structure. Genome Biology 12: R48.

Notes added after-the-fact. Students of the genome landscape of Amborella trichopoda should read a review by Jonathan Wendel (2015) on polyploidy in plants.

"... Here I aim to highlight one key realization of this 'genomics era' in which we find ourselves, namely, that all modern flowering plant genomes derive from processes set in motion by a history of repeated, episodic whole-genome doubling or polyploidy" (page 1753, Wendel 2015).

Wendel, J. F. 2015. The wondrous cycles of polyploidy in plants. American Journal of Botany 102(11): 1753-1756.



Papaveraceae from a Gallic (Aptian) Potomac Group Member of North American Appalachia (December 2013):

Jud, N. A. and L. J. Hickey. 2013. Potomacapnos apeleutheron gen. et sp. nov., a new early Cretaceous angiosperm from the Potomac Group and its implications for the evolution of eudicot leaf architecture. American Journal of Botany 100(12): 2437-2449.

This paper should be read together with an important book chapter (D. W. Taylor and Hickey 1996), and the study by Barral et al. (2013) on the anatomy and paleophysiology of Iterophyllum lobatum (a basal eudicot) from the Neocomian (Barremian) La Huérguina Formation of the European Iberian Peninsula.

The image on the left side of this news clip is reproduced from Jud and Hickey (Figure 3, 2013) with the written permission of Professor Judy Jernstedt, Editor-in-chief of the American Journal of Botany, copyright ©2013.

"Potomacapnos apeleutheron gen. et sp. nov. 3, USNM 559298 (Holotype) showing two lobed leaflets with reticulate venation, intramarginal vein, and glandular teeth. The right leaflet has two major lobes and three lateral lobes. The left leaflet has one major lobe and one minor lobe preserved. The left leaflet is folded under and twisted about its axis 180°. It is 1–2 mm deeper in the matrix than the right leaflet. L: Major lobe, ll: lateral lobe. Scale bar = 5 mm."

Notes added after-the-fact. The following articles offer supplemental reading, which is necessary to place Potomacapnos apeleutheron within the context of evolution of Papaveraceae.

Barral, A., B. Gomez, T. S. Feild, C. Coiffard, and V. Daviero-Gomez. 2013. Leaf architecture and ecophysiology of an early basal eudicot from the early Cretaceous of Spain. Botanical Journal of the Linnean Society 173(4): 594-605.

Doyle, J. A. and G. R. Upchurch, Jr. 2014. Angiosperm clades in the Potomac Group: what have we learned since 1977? Bulletin of the Peabody Museum of Natural History 55(2): 111-134.

Friis, E. M., P. R. Crane, and K. R. Pedersen. 2011. Early Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press, 596 pp.

Jud, N. A. 2014. Morphotype catalog of a Zone I (Aptian-earliest Albian) Flora from Fairlington, Virginia, USA. Bulletin of the Peabody Museum of Natural History 55(2): 135-152.

Pérez-Gutiérrez, M. A., A. T. Romero-García, M. C. Fernández, G. Blanca, M. J. Salinas-Bonillo, and V. N. Suarez-Diego. 2015. Evolutionary history of fumitories (subfamily Fumarioideae, Papaveraceae): an old story shaped by the main geological and climatic events in the Northern Hemisphere. Molecular Phylogenetics and Evolution 88: 75-92.

Taylor, D. W. and L. J. Hickey. 1996. Chapter 9. Evidence for and implications of an herbaceous origin for angiosperms. Pp. 232-266 In: D. W. Taylor and L. J. Hickey (eds.), Flowering Plant Origin, Evolution, and Phylogeny. London: Chapman and Hall, 403 pp.



Holometabolous Larvae, Coleopterids, Hymenopterids, and Early Bugs from the Carboniferous (November 2013):

Nature publishes a letter by a team of entomologists and paleobiologists revealing "unexpected Pennsylvanian eumetabolan diversity."

"The data suggest that the foundations of the eventually hyperdiverse Holometabola, comprising most modern-day insect species, were already well established in the Pennsylvanian." (Letter, André Nel et al. 2013).

Nel, A., P. Roques, P. Nel, A. A. Prokin, T. Bourgoin, J. Prokop, J. Szwedo, D. Azar, L. Desutter-Grandcolas, T. Wappler, R. Garrouste, D. Coty, D. Huang, M. S. Engel, and A. G. Kirejtshuk. 2013. The earliest known holometabolous insects. Nature 503(7475): 257-261.

"The 'key innovation' of metamorphosis, present in holometabolan larvae and some Paraneoptera, may have fostered the longevity of these taxa during the Pennsylvanian climatic oscillations and the Permian-Triassic extinction event" (Letter, André Nel et al. 2013).

Canalization of form and lability of insect body size is tied-in with arthropod brain hormone secretions and the 20E-ecdysone cascade of larval metamorphosis. Paleobiological implications of a deeply conserved holometabolan molecular tool kit should take into account the recent review on how insect larvae sense their size:

Callier, V. and H. F. Nijhout. 2013. Body size determination in insects: a review and synthesis of size- and brain-dependent and independent mechanisms. Biological Reviews 88(4): 944-954.

Further, students should pay attention to results of insect rearing studies that report larval gustatory sensing of ecdysone, sugars, and secondary plant products. Do insect larvae sense plant brassinosteroids that are structurally similar to 20E-ecdysone?

Zhang, H.-J., C. P. Faucher, A. Anderson, A. Z. Berna, S. Trowell, Q.-M. Chen, Q.-Y. Xia, and S. Chyb. 2013. Comparison of contact chemoreception and food acceptance by larvae of polyphagous Helicoverpa armigera and oligophagous Bombyx mori. Journal of Chemical Ecology 39(8): 1070-1080.

Do brassinolides effect development of beetle and thrip larvae that feed in plant tissue galleries such as crevices in massive shoot apical meristems (SAMs)?

Thummel, C. S. and J. Chory. 2002. Steroid signaling in plants and insects - common themes, different pathways. Genes and Development 16(24): 3113-3129.



Palaeo-evo-devo in Land Plants, Giant Stomata of Bennettitaleans, and Angiosperm Origins (November 2013):

A significant Tansley Review on stomatal evolutionary-development (evo-devo) with a critical reappraisal of subsidiary cell character homology has been published in the New Phytologist.

Rudall, P. J., J. Hilton, and R. M. Bateman. 2013. Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants. New Phytologist 200(3): 598-614.

"Regarding the establishment of 'fossil fingerprints' as developmental markers for the regulation of stomatal patterning, we note that it is highly problematic to infer patterns of stomatal development based on the mere absence or presence of subsidiary cells in fossil cuticles" (page 610, Rudall et al. 2013).

This important review should be read together with three research articles on stomatal stem cell lineages, the seed plant cuticle tool kit and evolution of Class IV homeodomain leucine zipper genes in streptophytes.

Figure 1 on page 604 of Rudall et al. (2013) should be interpreted with caution as it is computed from older morphological character polarity and homology assessments, which are not supported by tool kit studies. As a class exercise to evaluate pitfalls of combined molecular and morphological phylogenies (see below), students have an opportunity to recompute seed plant evolutionary trees, and to calibrate these cladograms with fossils.



SEPALLATA Gene Expression, WGDs, and Neofunctionalization in the Monocot Floral Tool Kit (November 2013):

The Specht Lab has published a significant study of evo-devo in species of Zingiberales, which is important in understanding possible effects of paleopolyploidy on neofunctionalization of genes, gene regulatory networks (GRNs), and selection on monocotyledonous floral tool kit enzymes, polarity networks (PINs), and fertile short shoot morphologies.

Yockteng, R., A. M. R. Almeida, K. Morioka, E. R. Alvarez-Buylla, and C. D. Specht. 2013. Molecular evolution and patterns of duplication in the SEP/AGL6-like lineage of the Zingiberales: a proposed mechanism for floral diversification. Molecular Biology and Evolution 30(11): 2401-2422.

"This work contributes to a growing body of knowledge focused on understanding the role of gene duplications and the evolution of entire gene networks in the evolution of flower development" (Abstract, Yockteng et al. 2013).

Students of the evo-devo of cis-regulatory modules (CRMs), GRNs, and PINs of seed plant shoot apical meristems (SAMs) should take into account this review of theoretical approaches.

Alvarez-Buylla, E. R., E. Azpeitia, R. Barrio, M. Benítez, and P. Padilla-Longoria. 2010. From ABC genes to regulatory networks, epigenetic landscapes and flower morphogenesis: making biological sense of theoretical approaches. Seminars in Cell & Developmental Biology 21(1): 108-117.



Palynological Evidence of Flowering Plants from the Middle Triassic (Anisian) More Than 240 MYA (October 2013):

Yet another important study of pollen samples recovered from isolated sedimentary layers in [at least one] continuous stratigraphic sequence in two deep well cores, reports monosulcate, columellate palynomorphs, and Afropollis, from the Middle Triassic (Anisian) about 240 MYA.

Hochuli, P. A. and S. Feist-Burkhardt. 2013. Angiosperm-like pollen and Afropollis from the Middle Triassic (Anisian) of the Germanic Basin (Northern Switzerland). Frontiers in Plant Science, Plant Evolution and Development 4: Article 344.

The left-hand image is "PLATE I ¦ Scale bar[s] 10µm. (1), Pollen Type 1, specimen A, LM image (high focus)" (Hochuli and Feist-Burkhardt 2013): micrograph is reproduced by permission from Professor Peter A. Hochuli, Palaeontological Institute and Museum, University of Zürich, Zürich, Switzerland.

This study adds considerable weight to earlier work by these same authors (Hochuli and Feist-Burkhardt 2004), and to data reported by Bruce Cornet in the 1980s, suggesting a 100 million year old ghost lineage of enigmatic stem group angiosperms. Interestingly, the Weiach Bore Hole also yielded two types of Eucommiidites, extending the stratigraphic range of this well-known gymnosperm pollen form by more than 100 million years.

Hochuli, P. A. and S. Feist-Burkhardt. 2004. A boreal early cradle of angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). Journal of Micropalaeontology 23: 97-104.

"Whereas some authors considered it [Sanmiguelia] as an angiosperm [Brown 1956; Cornet 1986, 1989a] others suggested an attribution to ginkgophytes and rejected a possible relation to angiosperms [Crane 1987, Doyle and Donoghue 1993]" (Discussion-Cretaceous and Pre-cretaceous Records, Hochuli and Feist-Burkhardt 2013).

Definitive paleontological evidence published by Peter Hochuli and Susanne Feist-Burkhardt should be read together with a Sidney Ash and Stephen Hasiotis review of Sanmiguelia paleobiology, and their report of three new localities from the Blue Mesa Member (Norian) of the Lower Triassic Chinle Formation of southwestern North America.

Ash, S. R. and S. T. Hasiotis. 2013. New occurrences of the controversial late Triassic plant fossil Sanmiguelia Brown and associated ichnofossils in the Chinle Formation of Arizona and Utah, USA. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 268(1): 65-82.

Based on gene expression studies of extant angiosperm species does the foliar morphology, stem anatomy, and growth habit of Sanmiguelia display the fingerprint of an "ancestral developmental tool kit" (title, Floyd and Bowman 2007) of a monocotyledonous flowering plant?

Simply put, the wide-ranging and relatively abundant Norian Sanmiguelia should no longer be excluded from seed plant data sets and combined morphological- and molecular-phylogenetic analyses including possible use in calibration of tool kit phylogenies.

In 1985, Peter Crane presented an interesting idea namely, that some populations of late Paleozoic Vojnovskyales might have survived the end-Permian extinction (PTr) reappearing in the Triassic rock record as the seed plant Sanmiguelia.

"The male structures [of Sanmiguelia] appear to be strobili with sessile pairs of pollen sacs, more reminiscent of ginkgophytes than angiosperms, and the smooth monosulcate pollen has no angiosperm features" (page 319, J. A. Doyle 2012).

Doyle, J. A. 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40: 301–326.

Are certain Permo-carboniferous Ginkgophyta and Vojnovskyales paraphyletic gymnosperm clades tied-in with Triassic sanmiguelias and possible stem group angiosperms?

Finally, students of a Triassic origin of angiosperms and the paleopalynology of Afropollis should read two reviews by Doyle et al. (1990 [see page 1549]) and the book by Friis et al. (2011). Discovery of Afropollis in stratigraphically precise layers of Triassic sediments by Hochuli and Feist-Burkhardt (2013) confounds a phylogeny of the pollen of Winteraceae proposed by James A. Doyle and coworkers (Figure 2 on page 1562), clouds serious consideration of Caytoniales as possible flowering plant antecedents, and obviates a Neocomian (mid-Hauterivian) origin of flowering plants suggested by Friis et al. (2011).

Doyle, J. A., C. L. Hotton, and J. V. Ward. 1990. Early Cretaceous tetrads, zonasulculate pollen, and Winteraceae. I. Taxonomy, morphology, and ultrastructure. American Journal of Botany 77(12): 1544-1557.

Doyle, J. A., C. L. Hotton, and J. V. Ward. 1990. Early Cretaceous tetrads, zonasulculate pollen, and Winteraceae. II. Cladistic analysis and implications. American Journal of Botany 77(12): 1558-1568.

Friis, E. M., P. R. Crane, and K. R. Pedersen. 2011. Early Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press, 596 pp.



Evidence of Paleopolyploidy in Conifers: Preadaptation to Climate of the Triassic Hot House (October 2013):

Volume 280, Number 1768 of the Proceedings of the Royal Society of London, Series B, Biological Sciences (2013) publishes data on a Classopollis myerianus palynofloral zone of the Whitmore Point Member of the Triassic Moenave Formation of southwestern North America.

Kürschner, W. M., S. J. Batenburg, and L. Mander. 2013. Aberrant Classopollis pollen reveals evidence for unreduced (2n) pollen in the conifer family Cheirolepidiaceae during the Triassic-Jurassic transition. Proceedings of the Royal Society of London, Series B, Biological Sciences 280(1768): 20131708.

Cheirolepidiaceae were abundant and morphologically diverse Araucaria- or Cupressus-like shrubs and trees indigenous to forests of Triassic Pangaea, which were dispersed as the supercontinent split following the eruption of the Central Atlantic Magmatic Province (CAMP) to Gondwanan and Laurasian places of later Jurassic and Cretaceous times. Classopollis (unique conifer pollen with angiosperm-like exine and tectate columellae) were shed from cones of male plants and dispersed by wind to fleshy bitegmic ovules on cone scales of mother shrubs and trees, which were indigenous to coastal terrestrial habitats (pages 831-838, T. N. Taylor et al. 2009).

Detailed paleobiological studies by Wolfram Kürschner et al. (2013) constitute the first report of unreduced gamete formation (inferred from light microscopic study of dispersed pollen) in a vascular plant, which dovetails with molecular-phylogenetic modeling by Jiao et al. (2011) documenting a swarm of whole genome duplications (WGDs) in seed plants, about 192 MYA:

Jiao, Y., N. L. Wickett, S. Ayyampalayam, A. S. Chanderbali, L. Landherr, P. E. Ralph, L. P. Tomsho, Y. Hu, H. Liang, P. S. Soltis, D. E. Soltis, S. W. Clifton, S. E. Schlarbaum, S. C. Schuster, H. Ma, J. Leebens-Mack, and C. W. dePamphilis. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345): 97-100.

Can paleobotanists find anatomical evidence of paleopolyploidy in hybridizing populations of the most recent common ancestor (MRCA) of extant seed plants, which were indigenous Euramerican cratons and island paleoenvironments of the early Carboniferous icehouse, to verify the alpha- (α-) peak of seed plant WGDs, about 319 MYA? Some allopolyploids might have been angiosperm sister groups to conifers, cycads, ginkgophytes, and gnetophytes of the Permo-carboniferous.

Yet, some paleobotanists suggest a monophyletic origin of flowering plants in the Jurassic or Cretaceous, a hypothesis which is based on APG IV (2016) combined with problematic morphological-phylogenetic data. Long-branch attraction may be prevalent in APG IV and more specific molecular-phylogenetic analyses.

Angiosperm Phylogeny Group (APG) IV could be refined and further supported by including fossil calibrations and molecular-phylogenetic analyses of seed plant homeodomain proteins, tool kit enzymes, and by incorporating studies of mobile transcription factors (TFs).

Notes added after-the-fact. The Triassic hot house and prolonged bouts of disruption to the biosphere from volcanic gases and volatile hydrocarbons ostensibly affecting terrestrial vegetation, including reproduction in coniferous plant populations, is discussed on pages 335-337 of Van De Schootbrugge and Wignall (2. The atmosphere, 2.a. Atmospheric Pollution, page 338, 2016).

"... increased UV radiation from decreased ozone shielding [exacerbated by volcanic outgassing and induced volatiles] may have triggered malformations in plant reproductive systems ..." (page 346, 5. Converging scenarios: similarities and differences, Van De Schootbrugge and Wignall 2016 [phrase in brackets is mine]).

Color illustrations of malformed Classopollis pollen may be found in Figure 3c, 3d on page 338 of Van De Schootbrugge and Wignall (2016).

Background Reading:

APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20.

Benton, M. J. and R. J. Twitchett. 2003. How to kill (almost) all life: the end-Permian extinction event. Trends in Ecology and Evolution 18(7): 358-365.

Erwin, D. H. 2006. Extinction: How Life on Earth Nearly Ended 250 Million Years Ago. Princeton: Princeton University Press, 306 pp.

Knoll, A. H., R. K. Bambach, J. L. Payne, S. Pruss, and W. W. Fischer. 2007. Paleophysiology and end-Permian extinction. Earth and Planetary Science Letters 256(3-4): 295-313.

Pálfy, J. 2003. Volcanism of the Central Atlantic Magmatic Province as a potential driving force in the end-Triassic mass extinction. Pp. 255-267 In: W. Hames, J. G. Mcgone, P. Renne, and C. Ruppel (eds.), The Central Atlantic Magmatic Province: Insights from Fragments of Pangea. Washington, D. C.: American Geophysics Union.

Pálfy, J., A. Demény, J. Haas, M. Hetényi, M. J. Orchard, and I. Vetõ. 2001. Carbon isotope anomaly and other geochemical changes at the Triassic-Jurassic boundary. Geology 29: 1047-1050.

Van De Schootbrugge, B. and P. B. Wignall. 2016. A tale of two extinctions: converging end-Permian and end-Triassic scenarios. Geological Magazine 153(2): 332-354.

Wignall, P. B. 2015. The Worst of Times: How Life on Earth Survived 80 Million Years of Extinctions. Princeton: Princeton University Press, 199 pp.

I thank Ralph Molnar, Ph.D. for bringing Professor Wignall's book to my attention.



Gene Expression Studies of Spruce Illuminate Conifer Cone Organ Homologies in Deep Time (October 2013):

Carlsbecker, A., J. F. Sundström, M. Englund, D. Uddenberg, L. Izquierdo, A. Kvarnheden, F. Vergara-Silva, and P. Engström. 2013. Molecular control of normal and acrocona mutant seed cone development in Norway spruce (Picea abies) and the evolution of conifer ovule-bearing organs. New Phytologist 200(1): 261-275.

"Our morphological and gene expression analyses give support to the hypothesis that the modern cone is a complex structure, and the ovuliferous scale the result of reductions and compactions of an ovule-bearing axillary short shoot in cones of Paleozoic conifers" (page 261, Carlsbecker et al. 2013).

A commentary (Ruelens and Geuten 2013) on this study by Peter Engström and coworkers, discusses spur shoot-like ovuliferous organ development in Picea abies var. acrocona mutants within the context of Permian Pseudovoltzia liebeana and Thuringiostrobus florinii cone anatomy and expression patterns of angiosperm LFY and the SEP (MIKC-type MADS-box E) gene family.

Ruelens, P. and K. Geuten. 2013. When paleontology and molecular genetics meet: a genetic context for the evolution of conifer ovuliferous scales. New Phytologist 200(1): 10-12.

"... the phylogeny of gymnosperms and their relationship to flowering plants remains debated as morphological and molecular analyses contradict each other on key relationships" (page 10, Ruelens and Geuten 2013).

Students of seed plant evolution have an opportunity to reassess character homologies and to recompute combined morphological and tool kit phylogenies calibrated by fossils, which may encourage classroom debate on the origin of flowering plants.



Contrasting Patterns of Stomatal Development in Basal Angiosperms Confirmed by Ultrastructure (October 2013):

Rudall and Knowles (page 1032, 2013) state an important caveat:

"Developmental studies of these phylogenetically pivotal taxa [Amborella, Austrobaileya, Schisandra] are essential to understand both the homologies of stomatal types and the evolution of stomatal development in angiosperms."

Rudall, P. J. and E. V. W. Knowles. 2013. Ultrastructure of stomatal development in early-divergent angiosperms reveals contrasting patterning and pre-patterning. Annals of Botany 112(6): 1031-1043.

This study confirms that some water-lilies (Nymphaeales) lost stomate developmental asymmetry while Amborella and Austrobaileya retain the putatively plesiomorphic character state, which is paracytic resulting from "... at least one asymmetric [cell] division ..."

More data from extant and fossil magnoliids and monocots are needed in order to shed light on ancestral character states of subsidiary cells and to understand stomatal evo-devo from ecophysiological and tool kit perspectives.



Major Trends in Vein Packing and Hydraulic Function in Early Angiosperms Are Evident (August 2013):

Feild, T. S. and T. J. Brodribb. 2013. Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks. New Phytologist 199(3): 720-726.

When "Baileyan trends," are revealed from future analyses of innovative third and fourth order venation patterns, high DV, and complex hydraulic conduit microstructure (including protoxylem, metaxylem, and a 2° vascular cambium) documented in thin-sectioned, permineralized Gnetum-like Permian leaves, does Figure 2 on page 723 of Feild and Brodribb (2013) become more intriguing?

Angiosperm-like fossilized leaves, midribs, and wood of Permian gigantopterids (seed plants incertae cedis), which were not studied by Feild and Brodribb (2013), have been discussed by Wilson and Knoll (2010).

"... vegetative features of gigantopterids suggest that they may resemble medullosans and angiosperms in functional [morpho] space, rather than conifers" (page 350, Wilson and Knoll 2010)

Wilson, J. P. and A. H. Knoll. 2010. A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants. Paleobiology 36: 335-355.

Despite the well-known fact that some clades of plants with vessels existed in the Permian Period, including gigantopterid seed plants with "physiologically explicit [hydraulic] morphospace" (the word in [brackets] is mine), Feild and Brodribb suggest:

"... angiosperms represent the only clade that evolved a xylem conduit anatomy sufficiently conductive to permit miniature vessels to maintain water supply ..." (page 723, Feild and Brodribb 2013)

Why not execute a paleobiological project to follow Boyce and Knoll (2002) and Boyce (2005), which is necessary to document examples of anatomical, hydraulic, and foliar innovations in seed plants indigenous to Permian terrestrial paleoenvironments, and to conduct phylogenetic tests of possible xylem heterochronies, calibrated by Delnortea fossils?

Notes added after-the-fact. Certain students of angiosperm paleophysiology seemingly downplay or strangely overlook anatomical evidence of high-vein densities in at least one Permian gymnosperm species (see below).

"... the results presented here suggest gymnosperms may have been constrained in the geological past [by seasonal water availability] because they never possessed high vein densities ..." (4. Discussion [a] limits on the ecological possibilities of ferns and gymnosperms, Zwieniecki and Boyce [2014], the comment in [brackets] is mine).

Three-dimensionally preserved secondary phloem and xylem of a permineralized leaf midrib of Delnortea abbottiae shown in Figures 23-36 on pages 1418 and 1420 of Mamay et al. (1988) is unequivocal evidence disputing the preceding statement.

Boyce, C. K. 2005. Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31(1): 117-140.

Boyce, C. K. and A. H. Knoll. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28(1): 70-100.

Mamay, S. H., J. M. Miller, D. M. Rohr, and W. E. Stein, Jr. 1988. Foliar morphology and anatomy of the gigantopterid plant Delnortea abbottiae from the Lower Permian of West Texas.  American Journal of Botany 75(9): 1409-1433.

Zwieniecki, M. A. and C. K. Boyce. 2014. Evolution of a unique anatomical precision in angiosperm leaf venation lifts constraints on vascular plant ecology. Proceedings of the Royal Society of London, Series B, Biological Sciences 281: 20132829.



MADS-box B Sister TFs in Bitegmic Ovules of Ginkgo Function in Development of a Fruit-like Organ (August 2013):

Lovisetto, A., Guzzo, F., Busatto, N., and G. Casadoro. 2013. Gymnosperm B-sister genes may be involved in ovule/seed development and, in some species, in growth of fleshy fruit-like structures. Annals of Botany 112(3): 535-544.

According this genetic study ... "a strong level of [MADS-box B sister] expression was maintained throughout the ovule [of Ginkgo biloba] also in later stages of development, when a layered organization of the integument had clearly developed, and both the inner and the outer integuments could be distinguished [Fig. 2H]" (page 537, Lovisetto et al. 2013).

Conversely, can ategmic ovules develop by fusion of integuments? Yes, according to R. H. Brown et al. (2010).

Brown, R. H., Nickrent, D. L. and C. S. Gasser. 2010. Expression of ovule and integument-associated genes in reduced ovules of Santalales. Evolution and Development 12(2): 231-240.

Is the bitegmic ovule an angiosperm-specific character? No.

Based on gene expression data and studies of plant development in extant model plant species, should paleobotanists reconsider homologies of angiosperm and ginkgoalean integuments and a common evo-devo of ovules attached to megasporophylls of reproductive spur shoots?



RAM Organization in Nymphaeales Is Similar to Acorales While Amborella Roots Are Eudicot-like (July 2013):

Oxford Journals publishes a review on root apical meristem (RAM) evo-devo in angiosperms.

Seago, J. L., Jr. and D. D. Fernando. 2013. Anatomical aspects of angiosperm root evolution. Annals of Botany 112(2): 223-238.

What is the putative relationship of mycorrhizal fungi to strigolactones and the RAM tool kit when placed in an ecological and phylogenetic context? Students can mine more information in this same issue of the Annals of Botany, and from discussion in a book chapter written by Koltai et al. (2012).

Notes added after-the-fact. Definitive fossilized evidence of a growing seed plant RAM, which is complete with permineralized stem cells, procambium, and Körper-Kappe, is reported from a >300 million-year-old coal ball (Hetherington et al. 2016). The Guardian publishes a news story on this extraordinary fossil find.

"... Comparison of the cellular organization of the different regions of the root apex indicates that the cellular dynamics [root cap] in R. carbonica conforms to that in extant root apical meristems [RAMS] ..." (Results and Discussion on page 1629 of Hetherington et al. [2016], words in [brackets] are mine).

Discovery of the Radix RAM spawns more questions than answers, in my opinion. First and foremost, study of the root anatomy of Amborella trichopoda reveals a derived stem cell structure, which is eudicot-like.

Since the permineralized RAM of Radix carbonica is different from any known but extant gymnosperm, what can paleobotanists and plant biologists conclude from its fingerprint of developmental regulation?

Were Radix carbonica roots once attached to a callistophytalean or vojnovskyalean seed plant rooted in a Carboniferous swamp?

Were vesicular-arbuscular mycorrhizal (VAM) fungi associated with these seed plants? And what, if any, potential strigolactone hormonal interactions existed between possible seed plant-VAM associations of Carboniferous paleoenvironments.

Background Reading:

Hetherington, A. J., J. G. Dubrovsky, and L. Dolan. 2016. Unique cellular organization in the oldest root apical meristem. Current Biology 26: 1629-1633.

Koltai, H. L. 2013. Strigolactones activate different hormonal pathways for regulation of root development in response to phosphate growth conditions. Annals of Botany 112(2): 409-415.

Koltai, H., R. Matusova, and Y. Kapulnik. 2012. Strigolactones in root exudates as a signal in symbiotic and parasitic interactions. Pp. 49-73 In: J. M. Vivanco and F. Baluška (eds.), Secretions and Exudates in Biological Systems, Signaling and Communication in Plants Volume 12. New York: Springer, 283 pp.



DNA-binding LFY Protein and Auxin Comprise Modules Determining Floral Primordia in Malvid SAMs (May 2013):

The Society of Experimental Biology publishes another important study on the evo-devo of SAM primordia and the floral tool kit.

Chahtane, H., G. Vachon, M. Le Masson, E. Thévenon, S. Périgon, N. Mihajlovic, A. Kalinina, R. Michard, E. Moyroud, M. Monniaux, C. Sayou, V. Grbic, F. Parcy, and G. Tichtinsky. 2013. A variant of LEAFY reveals its capacity to stimulate meristem development by inducing RAX1. The Plant Journal 74(4): 678-689.

A related paper from the recent archives of Cell Press sheds light on the biochemistry of LEAFY genes, auxins, and TFs in malvids:

Yamaguchi, N., M.-F. Wu, C. M. Winter, M. C. Berns, S. Nole-Wilson, A. Yamaguchi, G. Coupland, B. A. Krizek, and D. Wagner. 2013. A molecular framework for auxin-mediated initiation of flower primordia. Developmental Cell 24(3): 271-282.

A growing body of biochemical and morphological evidence suggests that cones and flowers are reproductive short shoots. Fertile spur shoots are demonstrably ancient organs known from Permo-carboniferous seed plant fossils. Further, numerous molecular phylogenetic studies of homeodomain proteins and TFs posit deep conservation of cone and floral CRMs, GRNs and PINs.

Can we compute a molecular phylogeny of LFY enzyme and its DNA-binding homeodomain, which is calibrated by fossils of cones and protoflowers, to better understand starting points of floral tool kit function and to discern evolutionary patterns in deep time?



Annual Review of Earth and Planetary Sciences Discusses Late Paleozoic Insect-Plant Associations (May 2013):

Labandeira, C. C. and E. D. Currano. 2013. The fossil record of plant-insect dynamics. Annual Review of Earth and Planetary Sciences 41: 287-311.

The most recent review on paleoherbivory and recovery of Permian landscapes following global biotic crises is published by Annual Reviews.

A second review in this volume by Montañez and Poulsen on the demise of the Upper Devonian and Lower Carboniferous icehouse should set a stage for interacting arthropods and seed plants of the Permo-triassic hothouse.

Montañez, I. P. and C. J. Poulsen. 2013. The late Paleozoic ice age: an evolving paradigm. Annual Review of Earth and Planetary Sciences 41: 629-656.



Evolutionarily Advanced Magnoliales and Nymphaeales from a Gondwanan Crato Paleoflora (February 2013):

Clément Coiffard and co-workers report a definitive fossil find of crown group Nymphaeales from the early Cretaceous South American Crato Formation.

Coiffard, C., B. A. Mohr, and M. E. C. Bernardes-de-Oliveira. 2013. Jaguariba wiersemana gen. nov. et sp. nov., an early Cretaceous member of crown group Nymphaeales (Nymphaeaceae) from northern Gondwana. Taxon 62(1): 141-151.

The left-hand image is Figure 1B on page 144 of Coiffard et al. (2013), "Jaguariba wiersemana gen. nov. et sp. nov.: morphology. B, complete plant, paratype (1999/615)." The scale bar at the lower right of the image is 1 cm.

Figure 1B is reproduced by permission from the International Association for Plant Taxonomy, Bratislava, Slovak Republic through Professor Joachim W. Kadereit, Editor-in-chief of Taxon, which is the "international journal of taxonomy, phylogeny and evolution," copyright ©2013.

This original research work should be read together with Barbara Mohr et al. (2013) on the discovery of the novel magnolialean species, Schenkeriphyllum glanduliferum from the Crato beds, to include revisiting important earlier discussions on biogeography, character evolution, and paleobotany of magnoliids by Bernhardt, Dilcher, J. A. Doyle, Endress, R. M. K. Saunders, Thien, and others (citations and discussion in the links to articles and the essay):

Mohr, B. A., C. Coiffard, and M. E. C. Bernardes-de-Oliveira. 2013. Schenkeriphyllum glanduliferum, a new magnolialean angiosperm from the early Cretaceous of northern Gondwana and its relationships to fossil and modern Magnoliales. Review of Paleobotany and Palynology 189: 57-72.

Together with Endressinia brasiliana these magnoliids possess putatively secreting staminodia not unlike extant Calycanthaceae, Degeneriaceae, and Eupomatiaceae. Many questions surface from morphological-phylogenetic, paleobotanical, and stratigraphic studies of South American sedimentary deposits of Gondwana by Clément Coiffard, Barbara Mohr, and others:

Can the Mohr et al. morphological-phylogenetic analysis (page 66-68, plate IX, 2013) of South American Crato Endressinia and Schenkeriphyllum, including Australasian Galbulimima (Himantandraceae, Magnoliales, Magnolianae) and Fijian Degeneria allow for a phylogeographic understanding of the paleobiology of common ancestors of these four Gondwanan genera with Laurasian magnoliids?

Do discoveries of fossilized remains from the Lower Cretaceous Crato Formation, which are referable to modern Nymphaeanae and core Magnolianae open a window to better understand origins and paraphyletic lines of evolution in basal flowering plants and magnoliids? Does the discovery of early Cretaceous fossil aroids including Spixiarum kipea from the Crato Paleolake complicate APG III after calibrating the basal angiosperm-monocot split?

Coiffard, C., B. A. Mohr, and M. E. C. Bernardes-de-Oliveira. 2013. The early Cretaceous aroid, Spixiarum kipea gen. et sp. nov., and implications on early dispersal and ecology of basal monocots. Taxon 62(5): 997-1008.

Further, does a supposed monophyletic origin of these geographically widespread, harmonic flowering plant groups with a derived (phenotypically specialized and genomically miniaturized) New Caledonian endemic Amborella trichopoda make evolutionary and phylogeographic sense, taking into account Loren Kroenke's neglected review of the complex and intriguing Mesozoic tectonic history of the southwest Pacific Basin with blocks of ancient, buried continental crust and shifting systems of ocean basins, island arcs, and subduction zones?

Kroenke, L. W. 1984. Chapter 2. New Caledonia: the Norfolk and Loyalty ridges; the New Caledonia and Loyalty Basins. Pp. 15-28 In: Cenozoic Tectonic Development of the Southwest Pacific. United Nations ESCAP, CCOP/SOPAC Technical Bulletin No. 6.



Cytochrome P450 Theme Issue Is Published by The Royal Society (February 2013):

Volume 368, Number 1612 of the Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences (2013), edited by David R. Nelson, is devoted to a discussion of the ancient protein family of cytochrome P450 enzymes.

Animals, fungi, microbes, and plants contain more than 18,000 molecular configurations of these fascinating enzymes, which are involved in the biosynthesis of anthocyanins, cutin, lignin, sporopollenin, steroids, suberin, and terpenoids, including compounds at the heart of the "chemical arms race."

These enzymes often act in concert with R2R3 myeloblastosis (MYB) transcription factors (TFs) involved in the catalysis of flavonoid biosynthesis. Flavonoids are important signaling molecules in seed plants, which interact with the PIN proteins of auxin regulation. Anthocyanins and flavonols are localized in epidermal cone cells and nectar guides of flower petals acting as optical cues for insect and bird pollinators.

Based on extreme conservation of R2R3 MYB homeodomain oncoproteins and some cytochrome P450s, were Paleozoic protoflowers colored and visualized by flying insects such as paleodictyopterans?



Cold Spring Harbor Symposium Book Volume on The Biology of Plants Is Available (January 2013):

The Cold Spring Harbor Laboratory held a symposium from May 30 to June 4, 2012 titled, "The Biology of Plants." Four of the workshop contributions, among others, are important toward a better understanding of the evo-devo of seed plant organs, ecophysiology and character homologies of the stomatal apparatus, and paleobiology of the pollination mutualism.

Bolduc, N., D. O'Connor, J. Moon, M. Lewis, and S. Hake. 2012. How to pattern a leaf. Cold Spring Harbor Symposia on Quantitative Biology 77: 47-51.

Plavskin, Y. and M. C. P. Timmermans. 2012. Small RNA-regulated networks and the evolution of novel structures in plants. Cold Spring Harbor Symposia on Quantitative Biology 77: 221-233.

Sheehan, H., K. Hermann, and C. Kuhlemeier. 2012. Color and scent: how single genes influence pollinator attraction. Cold Spring Harbor Symposia on Quantitative Biology 77: 117-133.

Wengler, D. L. and D. C. Bergmann. 2012. On fate and flexibility in stomatal development. Cold Spring Harbor Symposia on Quantitative Biology 77: 53-62.



Macmillan Publishers News of a Preserved Arthropod Brain from Cambrian Rocks (October 2012):

Nature publishes a letter by a team of entomologists and paleobiologists having a bearing on the evo-devo of neuropils associated with the brain, and homologies with sensory organs of advanced crustaceans and insects:

Ma, Xiaoya, Xianguang Hou, G. D. Edgecombe, and N. J. Strausfeld. 2012. Complex brain and optic lobes in an early Cambrian arthropod. Nature 490(7419): 258-262.

A fossilized brain from a Cambrian stem group arthropod is evidence of the early existence of an extremely conserved and sophisticated olfactory and visual sensory system in these animals ... Did evo-devo of insect eyes, mushroom bodies, neuropils, and trichromatic vision predate late Paleozoic pollen phytophagy and flying predatory behaviors of paleodictyopterans and wasps?

The left-hand image is reproduced from Figure 1 on page 258 of X. Ma et al. (2012), "Fuxianhuia protensa from the Chengjiang Lagerstätte. Dorsal view of complete specimen, YKLP 11321. A1, antenna; Ab, abdomen; Es, eye stalk; Ey, eye; Hs, head shield; Oc, optic capsule; Th, thorax. Scale bar, 1 cm." Figure 1 is licensed and reprinted by permission from Macmillan Publishers Ltd and the journal Nature, copyright ©2012.

Ecologists should compare this paleobiological study with earlier work by Chittka (1996), Briscoe and Chittka (2001), and Chittka et al. (2001). Implications of these three studies toward an understanding of the deep time evolution of pollination mutualisms and color and scent perception by species of the "Big Five" holometabolous insect orders and late Paleozoic seed plants, when taking into account the paleobiology of the arthropod brain, are absolutely profound.

"It is likely that trichromacy existed prior to the advent of angiosperm flowers" (page 138, Chittka 1996).

Briscoe, A. D. and L. Chittka. 2001. The evolution of color vision in insects. Annual Review of Entomology 46: 471–510.

Chittka, L. 1996. Does bee color vision predate the evolution of flower color? Naturwissenschaften 83: 136-138.

Chittka, L., J. Spaethe, A. Schmidt, and A. Hickelsberger. 2001. 6. Adaptation, constraint, and chance in the evolution of flower color and pollinator color vision. Pp. 106-126 In: L. Chittka and J. D. Thomson (eds.), Cognitive Ecology of Pollination, Animal Behaviour and Floral Evolution. Cambridge: Cambridge University Press, 344 pp.

Protoflowers known only from fragments and detached megasporophylls were probably modifications of developmentally plastic bisexual cone axes representing divergent clades of several Permian gymnosperms that survived the end-Permian apocalypse. When supported by paleobotanical evidence, were anthocyanic, pinwheel shaped fertile short (spur) shoots of Permo-carboniferous seed plants visually discernable to pollinivores, paleodictyopterans, and predatory wasps?

"Hence, a flower that stands out against green foliage can be predicted to be equally conspicuous against brown soil, grey stones and other inorganic backgrounds" (page 1505, Chittka et al. 1994).

Chittka, L., A. Schmidt, N. Troje, and R. Menzel. 1994. Ultraviolet as a component of flower reflections, and the colour perception of Hymenoptera. Vision Research 34: 1489-1508.

Notes added after-the-fact. Paleobiological studies of the early Paleozoic arthropod brain continue as evidenced by the publication of two significant follow-up papers.

Edgecombe, G. D., Xiaoya Ma, and N. J. Strausfeld. 2015. Unlocking the early fossil record of the arthropod central nervous system. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 370(1684): DOI 10.1098/rstb.2015.0038.

Ma, Xiaoya, G. D. Edgecombe, Xianguang Hou, T. Goral, and N. J. Strausfeld. 2015. Preservational pathways of corresponding brains of a Cambrian euarthropod. Current Biology 25(22): 2969-2975.



Annals of Botany Publication on Secondary Pollen Receptive Surfaces (August 2012):

Transferential stigmatic tool kit function to a foliar organ of an angiosperm flower ... can petals act as male-receptive female organs? Oxford Journals publishes a paper by a team of entomologists and plant biologists having a bearing on the evo-devo of the carpel and evolution of a pollination mutualism with the foliar organ of a monocot flower.

Johnson, S. D., A. Jürgens, and M. Kuhlmann. 2012. Pollination function transferred: modified tepals of Albuca (Hyacinthaceae) serve as secondary stigmas. Annals of Botany 110(3): 565-572.



Annual Review of Earth and Planetary Sciences Publishes Research on the Origin of Flowering Plants (May 2012):

Doyle, J. A. 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40: 301–326.

The most recent review to date on the origin of flowering plants is published by Annual Reviews. The review is the latest installment of Professor Doyle's more than 35 years of research on the origin of angiosperms, which should be read together with a lavishly-illustrated and widely-acclaimed book by Friis et al. (2011).

Notes added after-the-fact. Colleagues and students might wonder why Professor Emeritus J. A. Doyle's thoughtful essay was not selected as Gigantopteroid "Outstanding Publication of Year 2012." My reasons are encapsulated by the following clear and to-the-point arguments.

Apparently, the intent of J. A. Doyle's review of molecular and paleobotanical evidence on the origin of angiosperms was to explore "areas of congruence and conflict and ways in which conflicts might be resolved ..." (page 302, Introduction, J. A. Doyle 2012). Elaborate discussion of 1986 and 1987 milestone syntheses (coauthored with M. J. Donoghue) is incongruent with seed plant organ homologies explained by Mathews and Kramer (2012).

Despite a 2006 discussion of YABBY transcription factors (TFs) and ovule determinants, J. A. Doyle skirts research advances on evolutionary-development (evo-devo) of molecular tool kits, which is a topic of considerable significance toward a deeper understanding of seed plant organ (including cone and floral) homologies based on developmental genetics (Mathews and Kramer 2012).

Yet, there is solid biochemical and morphological evidence that flowers are short- (spur-) shoots whose growth and development is orchestrated by intricate molecular machinery (the tool kit) comprised of cis-regulatory modules (CRMs), TFs, and gene-regulatory networks (GRNs) in germ cells of growing shoot apical meristems (SAMs).

Further, molecular phylogenetic studies of homeodomain proteins and TFs posit deep conservation of cone and floral CRMs, GRNs, auxin-based polarity networks (also supported by evidence from Permo-carboniferous fossils), efflux carriers, and PINs.

Actually, evo-devo including theoretical studies of floral shoot morphospace, and calibration of molecular tool kit phylogenies with fossils, might be novel approaches needed to resolve J. A. Doyle's dilemma.

Despite considerable discussion in the literature on angiosperm phylogeny and evolution by J. A. Doyle, Friis, and Frohlich, among others, Caytoniales and Petriellales probably had nothing to do with the "mysterious origin of flowering plants."

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

The image to the right and the figure legend below in quotation marks is from page 753 of Peter R. Crane (1985), Phylogenetic analysis of seed plants and the origin of angiosperms, Annals of the Missouri Botanical Garden 72: 716-796, reprinted with permission of the Missouri Botanical Garden and Peter Crane.

"Figure 17. Morphology of the Caytonia plant.
-A. Sagenopteris colpodes, based on Thomas (1925, pl. 15, fig. 50); × 0.75.
-B. S. colpodes, detail of leaflet attachment and venation, based on Harris (1964, fig. 2H); × 4.
-C. Caytonanthus arberi, based on Harris (1941, pl. 2, fig. 3); × 7.
-D. Pollen from C. arberi, based on Townrow (1962b, fig. 3d, e); × 1,200.
-E. Caytonia nathorstii megasporophyll, based on Harris (1964, fig. 10-A-C); × 5.
-F. Caytonia "cupule" containing seeds, based on Reymanowna (1973, particularly text fig. 12E, F); × 12.5.
-G. Caytonia "cupule," longitudinal section, based on Reymanowna (1973, particularly text fig. 12E, F); × 12.5.
-H. C. nathorstii ovule longitudinal section, redrawn from Harris (1958, fig. 7); × 110."

In view of Hochuli and Feist-Burkhardt's discovery of Afropollis (magnoliid pollen shed from possible Winteraceae), and angiosperm-like pollen from arid, boreal, and tropical paleoenvironments of Anisian time (2013), is the following statement accurate or precise?

"Despite nearly worldwide sampling, palynological studies failed to reveal angiosperm pollen before the mid-early Cretaceous, whereas some should have been transported from the uplands if angiosperms were growing there ..." (page 302, J. A. Doyle 2012).

Yet, well before J. A. Doyle tendered his proposal to the Annual Review of Earth and Planetary Sciences to write a follow-up review to earlier syntheses (J. A. Doyle and Donoghue 1986, 1987, J. A. Doyle 1994, 1996, 1998, 2001, 2006), several palynological investigations were published offering another point of view. Paleobiological studies by Cornet (1989), Cornet and Habib (1992), Hochuli and Feist-Burkhardt (2004), Zavada (2007), and Zavialova and Gomankov (2009) provided palynological data that contradict the J. A. Doyle statement published in 2012, quoted above.

Further, the paleoecologies of ancient flowering plant populations were probably not "xerophobic," "dark and disturbed," or "wet and wild." These are sophomoric ideas, which are perplexing to some paleobiologists in the halls of natural history museums, floated by certain students of paleophysiology.

Cornet, B. 1989. Late Triassic angiosperm-like pollen from the Richmond Rift Basin of Virginia. Palaeontographica B 213: 37-87.

Cornet, B. and D. Habib. 1992. Angiosperm-like pollen from the ammonite-dated Oxfordian (Upper Jurassic) of France. Review of Palaeobotany and Palynology 71: 269-294.

Doyle, J. A. 1994. Origin of the angiosperm flower: a phylogenetic perspective. Plant Systematics and Evolution (Supplement) 8: 7-29.

Doyle, J. A. 1996. Seed plant phylogeny and the relationships of Gnetales. International Journal of Plant Sciences 157(6 Supplement): S3-S39.

Doyle, J. A. 1998. Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. Molecular Phylogenetics and Evolution 9: 448-462.

Doyle, J. A. 2001. Significance of molecular phylogenetic analyses for paleobotanical investigations on the origin of angiosperms. The Palaeobotanist 50: 167-188.

Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. The Journal of the Torrey Botanical Society 133(1): 169-209.

Doyle, J. A. and M. J. Donoghue. 1986. Seed plant phylogeny and the origin of angiosperms: an experimental cladistic approach. Botanical Review (Lancaster) 52(4): 321-431.

Doyle, J. A. and M. J. Donoghue. 1987. The origin of angiosperms: a cladistic approach.  Pp. 17-49 in: E. M. Friis, W. G. Chaloner, and P. R. Crane, The Origin of Angiosperms and Their Biological Consequences.  Cambridge: Cambridge University Press, 358 pp.

Friis, E. M., P. R. Crane, and K. R. Pedersen. 2011. Early Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press, 596 pp.

Hochuli, P. A. and S. Feist-Burkhardt. 2004. A boreal early cradle of angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). Journal of Micropalaeontology 23: 97-104.

Mathews, S. and E. M. Kramer. 2012. The evolution of reproductive structures in seed plants: a re-examination based on insights from developmental genetics. New Phytologist 194(4): 910-923.

Zavada, M. S. 2007. The identification of fossil angiosperm pollen and its bearing on the time and place of the origin of angiosperms. Plant Systematics and Evolution 263: 117-134.

Zavialova, N. E. and A. V. Gomankov. 2009. Occurrence of angiosperm-like ultrastructural features in gymnosperm pollen from the Permian of Russia. Review of Palaeobotany and Palynology 156(1-2): 79-89.



Annual Review of Ecology, Evolution, and Systematics Revisits Ehrlich and Raven (December 2011):

Annual Reviews, a non-profit scientific organization, publishes a paper by Niklas Janz that critiques Paul Ehrlich and Peter Raven’s classic 1964 article on plant and lepidopteran mutualisms:

Janz, N. 2011. Ehrlich and Raven revisited: mechanisms underlying codiversification of plants and enemies. Annual Review of Ecology, Evolution, and Systematics 42: 71-89.



Yale University Research on the Triassic Origin of Flowering Plants (March 2010):

Molecular phylogenetic studies by Yale University colleagues suggest a late Triassic age for the flowering plant crown group (March 2010).

Smith, Stephen A., J. M. Beaulieu, and M. J. Donoghue. 2010. An uncorrelated relaxed-clock analysis suggests an earlier origin for flowering plants. Proceedings of the National Academy of Sciences 107(13): 5897-5902.

Contrary to assertions reported in the Science Daily, Stephen A. Smith et al. (2010) are not the first scientists to propose a Triassic origin of angiosperms. Bruce Cornet, Ph.D. should receive credit for his quite correct and detailed arguments in support of a Triassic origin of flowering plants, which appear in two papers published in 1986 and 1989.

Students have ample opportunities to compare and contrast relaxed-clock methods and to discuss Bayesian priors when comparing angiosperm and seed plant phylogenies computed by Bell et al. (2010) with Stephen A. Smith et al. (2010) and Magallón (2010).

Bell, C. D., D. E. Soltis, and P. S. Soltis. 2010. The age and diversification of the angiosperms revisited. American Journal of Botany 97: 1296-1303.

Magallón, S. 2010. Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms. Systematic Biology 59(4): 384-399.



Discussion Meeting Issue "Darwin and the Evolution of Flowers" (February 2010):

Volume 365, Number 1539 of the Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences (2010), edited by Peter R. Crane, Else Marie Friis, and William G. Chaloner is devoted to a discussion of Charles Darwin and the origin of flowers.

Fifteen articles are devoted to the topic including papers by:

Endress, P. A. 2010. The evolution of floral biology in basal angiosperms. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365(1539): 411-421.

Friis, E. M., K. R. Pedersen, and P. R. Crane. 2010. Diversity in obscurity: fossil flowers and the early history of angiosperms. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365(1539): 369-382.

Jasinski, S., A. C. M. Vialette-Guiraud, and C. P. Scutt. 2010. The evolutionary-developmental analysis of plant microRNAs. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365(1539): 469-476.

Mathews, S., M. D. Clements, and M. A. Beilstein. 2010. A duplicate gene rooting of seed plants and the phylogenetic position of flowering plants. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365(1539): 383-395.

Rudall, P. J. and R. M. Bateman. 2010. Defining the limits of flowers: the challenge of distinguishing between the evolutionary products of simple versus compound strobili. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 365(1539): 397-409.

Notes added after-the-fact. Students of paleobiology may wish to critique a curious little paper, which was published in the June 2016 issue of Cretaceous Research.

Cascales-Miñana, B., C. J. Cleal, P. Gerrienne. 2016. Is Darwin's 'Abominable Mystery' still a mystery today? Cretaceous Research 61: 256–262.

"We have examined herein different methodological approaches (i.e. fossil-based, molecular, phylogenetic and paleobiogeographic studies) and current viewpoints about the explosive Cretaceous diversification of angiosperms. After integrating evidence as a whole with our results, the resulting scenario suggests that there is nothing particularly mysterious about the diversification of angiosperms during Cretaceous times or how it is reflected in the fossil record. The clade probably first appeared during Triassic times, possibly as a result of the re-setting of plant evolutionary history following the devastating global extinction event of the Permian–Triassic boundary ..." (4. Conclusions, Cascales-Miñana et al. 2016).

The preceding statement is an optimistic appraisal of methodology used by Cascales-Miñana et al. (2016). Some "current viewpoints" are left out of the analysis. And the fossil dataset used by the Cascales-Miñana team is grossly incomplete.

Caytoniales and angiosperms diverged from a common ancestor with Bennettitales in the Lower Triassic according to Cascales-Miñana et al. (page 258, Figure 1, 2016). Yet, these authors assert that "... the [angiosperm] clade probably first appeared during Triassic times," which is a stratigraphic conundrum.

Why assume that angiosperms constitute a single clade first appearing 256 MYA without discussing Mathews (2009, see below) and Mathews et al. (2010)?

Seed plant phylogenies are potentially misleading. Some key studies on aspects of floral organ homologies (Christianson and Jernstedt 2009, Rudall and Bateman 2010) went unnoticed by Cascales-Miñana et al. (2016). Interestingly, the team admits that some seed plant groups are non-monophyletic.

Several competing seed plant phylogenies surfaced in the literature in the past 25 years but few take into account well-reasoned homologies based on evolutionary development (evo-devo) or mathematical scaling of nested organs of the reproductive shoot apical meristem (SAM), which begs several [albeit relentless] avenues of questioning.

Despite valiant attempts by Angiosperm Phylogeny Group [APG] IV to reconstruct a credible and defensible molecular-based cladogram for crown-group angiosperms (APG 2016), are flowering plants as a whole non-monophyletic?

Is the angiosperm flower homologous with short- [spur-] shoots of Permo-carboniferous seed plants such as Vojnovskyales?

If Hilton and Bateman (2006), "remains the best available [it is not, see Rothwell and Stockey 2016] model for seed-plant phylogeny that incorporates detailed paleobotanical evidence," (2.1 Plotting a time scaled phylogeny, page 27, Cascales-Miñana et al. 2016, phrase [in brackets] is mine), then why mine the Paleobiology Database when two possibly critical angiosperm stem lineages, sanmiguelias and vojnovskyaleans are left-out?

Are cone and floral tool kits are too conserved i.e. demonstrably Permo-carboniferous in origin to somehow accommodate bizarre reproductive morphologies seen in Caytoniales, Corystospermales, Glossopteridales, Pentoxylales, and Petriellales?

Why not adopt glossopterids as potential outgroup to the angiosperms, coniferophytes, cycadophytes, ginkgophytes, and gnetophytes?

Students of angiosperm phylogeny should not forget that Peter Crane (1985) once suggested that the foliage of Vojnovskyales resembled the Triassic monocot-like plant Sanmiguelia. The Cascales-Miñana team should pay attention to written accounts by Ash and Hasiotis (2013) of Sanmiguelia populations indigenous to arid Triassic landscapes.

Phylogenomics suggests Cretaceous co-radiations of Diptera, Hymenoptera, and Lepidoptera, and angiosperms. A milestone research report on the molecular systematics of insect nuclear genes by Misof et al. (2014) suggest Early Cretaceous "spectacular diversifications" of ants, bees, butterflies, moths, flies, and wasps with "the radiation of flowering plants."

Yet, the elaborate and "statistically-robust" phylogenomic study by Misof et al. (2014) is questioned in a later reanalysis of the data by K. Jun Tong et al. (2015), which employed Bayesian priors and added calibrations and discussion of paleoentomological evidence published in vast literature on insect fossils.

"... we estimate the ages of the megadiverse orders Diptera [flies] and Lepidoptera [butterflies and moths] at ≈266 and ≈263 Ma [million years ago], respectively. These are ≈100 My [million years] earlier than those of Misof et al. [2014]. Our estimates are consistent with the fossil record ... and challenge the hypothesis that these two orders diversified contemporaneously with angiosperms" (quoted from K. Jun Tong et al. 2015, words in brackets [] are mine).

A January 2015 special issue of Cretaceous Research (Volume 52 Part B, pages 313-630) publishes 36 papers on the diversity, palaeoecology and taphonomy of Cretaceous insects. Yet, citation of this work and discussion of Labandeira's 2014 book chapter is somehow overlooked by Cascales-Miñana et al. (2016). The lag time between submission of manuscripts to the Editorial Office of Cretaceous Research, receipt of peer reviewer comments, and delays in publication probably contributed to this oversight.

In my opinion, there are few reasons to leave out discussion of potentially important published scientific work, to reanalyze outdated morphological-phylogenetic seed plant cladistic exercises, or to incompletely harvest paleobiological data when attempting syntheses. The so-called "sudden" or "explosive" superradiation of flowering plants with animals including ornithischian dinosaurs and the "big five" palynivores and pollinators, is a prime example of a synthesis to be supported by thorough review of the literature coupled with infusion of novel ideas and statistically robust analyses of clean paleobiological datasets.

While it was not the intent of the Cascales-Miñana team to review the evolutionary relationships of seed plants with euornithopod transverse grinders and insect mutualists, choice of the Hilton and Bateman 2006 seed plant phylogeny, Misof team 2014 cladistic model, and Weishampel and Jianu 2000 study could affect outcomes shown in Figure 2 and invalidate certain conclusions.

There are many problems with the dataset used by Cascales-Miñana et al. (2016). Significant discussion of other papers published in the Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences (references listed above) and the Annual Review of Earth and Planetary Sciences (J. A. Doyle 2012, P. M. Barrett 2014), was left-out by the Cascales-Miñana team. Further, much more work is necessary to plot a solution to Darwin's so-called "mystery."

Further Reading:

APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 181: 1-20.

Ash, S. R. and S. T. Hasiotis. 2013. New occurrences of the controversial late Triassic plant fossil Sanmiguelia Brown and associated ichnofossils in the Chinle Formation of Arizona and Utah, USA. Neues Jahrbuch für Geologie und Paläontologie Abhandlungen 268(1): 65-82.

Barrett, P. M. 2014. Paleobiology of herbivorous dinosaurs. Annual Review of Earth and Planetary Sciences 42: 207-230.

Christianson, M. L. and J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: a quantitative analysis of the disposition of axillary structures. American Journal of Botany 96(11): 1957-1966.

Crane, P. R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanic Garden 72: 716-793.

Doyle, J. A. 1996. Seed plant phylogeny and the relationships of Gnetales. International Journal of Plant Sciences 157(6 Supplement): S3-S39.

Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. The Journal of the Torrey Botanical Society 133(1): 169-209.

Doyle, J. A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169(7): 816-843.

Doyle, J. A. 2012. Molecular and fossil evidence on the origin of angiosperms. Annual Review of Earth and Planetary Sciences 40: 301–326.

Hilton, J. and R. M. Bateman. 2006. Pteridosperms are the backbone of seed-plant evolution. Journal of the Torrey Botanical Society 133(1): 119-168.

Labandeira, C. C. 2014. Chapter 13. Why did terrestrial insect diversity not increase during the angiosperm radiation? Mid-Mesozoic, plant-associated insect lineages harbor clues. Pp. 261-299 In: P. Pontarotti (ed.), Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life. New York: Springer, 398 pp.

Misof, B., Shanlin Liu, K. Meusemann, R. S. Peters, A. Donath, C. Mayer, P. B. Frandsen, J. Ware, T. Flouri, R. G. Beutel, O. Niehuis, M. Petersen, F. Izquierdo-Carrasco, T. Wappler, J. Rust, A. J. Aberer, U. Aspöck, H. Aspöck, D. Bartel, A. Blanke, S. Berger, A. Böhm, T. R. Buckley, B. Calcott, Junqing Chen, F. Friedrich, M. Fukui, M. Fujita, C. Greve, P. Grobe, Shengchang Gu, Ying Huang, L. S. Jermiin, A. Y. Kawahara, L. Krogmann, M. Kubiak, R. Lanfear, H. Letsch, Yiyuan Li, Zhenyu Li, Jiguang Li, Haorong Lu, R. Machida, Y. Mashimo, P. Kapli, D. D. McKenna, Guanliang Meng, Y. Nakagaki, J. L. Navarrete-Heredia, M. Ott, Yanxiang Ou, G. Pass, L. Podsiadlowski, H. Pohl, B. M. von Reumont, K. Schütte, K. Sekiya, S. Shimizu, A. Slipinski, A. Stamatakis, Wenhui Song, Xu Su, N. U. Szucsich, Meihua Tan, Xuemei Tan, Min Tang, Jingbo Tang, G. Timelthaler, S. Tomizuka, M. Trautwein, Xiaoli Tong, T. Uchifune, M. G. Walz, B. M. Wiegmann, J. Wilbrandt, B. Wipfler, T. K. F. Wong, Qiong Wu, Gengxiong Wu, Yinlong Xie, Shenzh Yang, D. K. Yeates, K. Yoshizawa, Qing Zhang, Rui Zhang, Wenwei Zhang, Yunhui Zhang, Jing Zhao, Chengran Zhou, Lili Zhou, T. Ziesmann, Shijie Zou, Yingrui Li, Xun Xu, Yong Zhang, Huanming Yang, Jian Wang, Jun Wang, K. M. Kjer, and Xin Zhou. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346(6210): 763-767.

Nixon, K. C., W. L. Crepet, D. M. Stevenson, and E. M. Friis. 1994. A reevaluation of seed plant phylogeny. Annals Missouri Botanical Garden 81: 484-533.

Rothwell, G. W., W. L. Crepet, and R. A. Stockey. 2009. Is the anthophyte hypothesis alive and well? New evidence from the reproductive structures of Bennettitales. American Journal of Botany 96(1): 296-322.

Rothwell, G. W. and R. Serbet. 1994. Lignophyte phylogeny and the evolution of spermatophytes: a numerical cladistic analysis. Systematic Botany 19(3): 443-482.

Rothwell, G. W. and R. A. Stockey. 2016. Phylogenetic diversification of early Cretaceous seed plants: the compound seed cone of Doylea tetrahedrasperma. American Journal of Botany 103: 923-937.

Tong, K. Jun, S. Duchêne, S. Y. W. Ho, and N. Lo. 2015. Comment on "Phylogenomics resolves the timing and pattern of insect evolution." Science 349(6247): Research Technical Comment Number 487, Insect Phylogenomics.

Weishampel, D. B. and C.-M. Jianu. 2000. Chapter 5, Plant-eaters and ghost lineages: dinosaurian herbivory revisited. Pp. 123-143 In: H.-D. Sues (ed.), Evolution of Herbivory in Terrestrial Vertebrates: Perspectives from the Fossil Record. Cambridge: Cambridge University Press, 256 pp.



Archived News:

Charles Darwin Bicentennial issue of the American Journal of Botany (January 2009). The January 2009 issue of the American Journal of Botany explores the origin, evolution, and radiation of flowering plants. More than twenty articles are devoted to the topic.

Contributions to the revised Jepson Manual (July 2008). John and the original authors of The Jepson Manual: Higher Plants of California (Hickman 1993) have revised and submitted treatments of Anacardiaceae (Malosma, Pistacia, Rhus, Schinus, and Searsia), Cucurbitaceae (Brandegea, Citrullus, Cucumis, Cucurbita, and Marah), Lamiaceae (Acanthomintha, Glechoma, Hedeoma, Lycopus, Marrubium, Melissa, Moluccella, Nepeta, Poliomintha, Prunella, Salazaria, Satureja, and Teucrium), and Montiaceae (Calandrinia, Calyptridium [with C. Matt Guilliams], Cistanthe [with C. Matt Guilliams], Claytonia, Lewisia, and Montia), for The Jepson Manual: Vascular Plants of California, Second Edition.

Baldwin, B. G., D. H. Goldman, D. J. Keil, R. Patterson, T. J. Rosatti, and D. H. Wilken (eds.). 2012. The Jepson Manual: Vascular Plants of California, Second Edition. Berkeley: University of California Press, 1568 pp.


Systematics of Claytonia [Portulacaceae] (July 2006). John M. Miller, Ph.D. and Kenton L. Chambers, Ph.D. have published a taxonomic monograph titled, Systematics of Claytonia (Portulacaceae), culminating more than 40 years of research on a biogeographically significant group of flowering plants, which are indigenous to the mountain chains of Asia and North America.

The image to the right consists of several tetraploid plants of Claytonia parviflora subsp. parviflora from the Greenhorn Mountains of western North America.

Interested persons may order a copy of the hardbound Volume 78 of this serial through the American Society of Plant Taxonomists Business Manager. Booksellers, botanists, and buyers may also wish to consult the home page of Systematic Botany Monographs.



Death Valley desert blooms (April 2005). The 2005 bloom season was extraordinary on the floor and alluvial debris fans of Death Valley, a graben located east of the Panamint Mountains, Death Valley National Park, Inyo County, California, USA. The author and his associates visited the region in April 2005 and captured these images, among others.

To the left is an image of a Holocene debris fan of the Grapevine Mountains (the Panamint Mountains are to the right): the yellow color is a population of Geraea canescens (Asteraceae, Asterales, Asteranae). To the right is a close-up of Eremalche rotundiflora (Malvaceae, Malvales, Rosanae) photographed by Homer Hobi (who accompanied John together with Ed Dipesa, now deceased).


Fairy lantern field biology (April 2004). Together with Tim Armstrong, the author discovered a previously undocumented population of Calochortus pulchellus (Liliaceae, Liliales, Lilianae) from a volcanic plateau in southern Solano County, California, which is not far from the Willis Linn Jepson Ranch.

The Mount Diablo fairy lantern was previously known from Contra Costa County on Mount Diablo, a prominent mountain peak of the Diablo Range rising above the foothills south of the Carquinez Straits and Suisun Bay of western North America.

Students may wish to read about Calochortus pulchellus in recent biosystematic studies of some Calochortus species published by Bryan Ness in 1989 (Systematic Botany 14:495-505).


The massif pictured above is Cerro de la Encantada (Picacho del Diablo) as viewed from the crest of the Sierra San Pedro Mártir, also known as Cerro Providencia or "Hill of the Enchanted." Snow is visible in the foreground under sparse stands of Abies concolor (white fir), Pinus jeffreyi (Jeffrey pine), and Pinus lambertiana (sugar pine).

The "Mountain of Providence" or "Devil's Picacho" (elevation 3096 meters) is the detached and uplifted grano-diorite and tonalite block of the Peninsular Mountains of westernmost North America.


[ top ]



TOPICS FOR DEBATE AND DISCUSSION

  • A New Family of Evolutionarily Advanced "Unsolved" Ceratophyllales from the Barremian 125 MYA
  • Amborella Is American Association for the Advancement of Science (AAAS) Genome of the Year
  • Annals of Botany Publication on Secondary Pollen Receptive Surfaces
  • Annals of Botany Publishes Special Issue on Cone and Floral Development
  • Annual Review of Earth and Planetary Sciences Discusses Late Paleozoic Insect-Plant Associations
  • Annual Review of Earth and Planetary Sciences Publishes Research on the Origin of Flowering Plants
  • Annual Review of Ecology, Evolution, and Systematics Revisits Ehrlich and Raven
  • Bayesian Computational Molecular Simulations Support a Triassic Age Estimate for Angiosperms
  • Cold Spring Harbor Symposium Book Volume on The Biology of Plants Is Available
  • Contrasting Patterns of Stomatal Development in Basal Angiosperms Confirmed by Ultrastructure
  • Convergence in Kalligrammatids and Papilionoids, and Angiosperm Mutualisms with Holometabola
  • Cupules and Ovules Inside a Permineralized Compound Cone from North American Valanginian Rocks
  • Cytochrome P450 Theme Issue Is Published by The Royal Society
  • Discussion Meeting Issue "Darwin and the Evolution of Flowers"
  • DNA-binding LFY Protein and Auxin Comprise Modules Determining Floral Primordia in Malvid SAMs
  • Evidence of Paleopolyploidy in Conifers: Preadaptation to Climate of the Triassic Hot House
  • Evolution of a LFY Protein Homeodomain Unfolds in Streptophytes, Bryophytes, and Seed Plants
  • Evolutionarily Advanced Magnoliales and Nymphaeales from a Gondwanan Crato Paleoflora
  • Flower Fossil Posits a Jurassic Angiosperm Crown Bedeviling Doctrine and Confounding Phylogenies
  • Gene Expression Studies of Spruce Illuminate Conifer Cone Organ Homologies in Deep Time
  • High DNA Content, Karyology, and Unusual Microsporogenesis in ANA grade Hydatellaceae
  • Holometabolous Larvae, Coleopterids, Hymenopterids, and Early Bugs from the Carboniferous
  • Late Triassic (Carnian) Cycadophyte Foliar Organs and Naming Detached Taeniopteroid Fossils
  • Long Branches of Unknown Angiosperm Stem Taxa May Affect Resolution of ANA Grade Species
  • Macmillan Publishers News of a Preserved Arthropod Brain from Cambrian Rocks
  • MADS-box B Sister TFs in Bitegmic Ovules of Ginkgo Function in Development of a Fruit-like Organ
  • Major Trends in Vein Packing and Hydraulic Function in Early Angiosperms Are Evident
  • Palaeo-evo-devo in Land Plants, Giant Stomata of Bennettitaleans, and Angiosperm Origins
  • Paleoherbivory in a Lower Permian (Kungurian) Riparian Florule of Southwestern North America
  • Palynological Evidence of Flowering Plants from the Middle Triassic (Anisian) More Than 240 MYA
  • Papaveraceae from a Gallic (Aptian) Potomac Group Member of North American Appalachia
  • RAM Organization in Nymphaeales Is Similar to Acorales While Amborella Roots Are Eudicot-like
  • Reproductive Modules and Gametangial Programs in Welwitschia are Gnetalean Synapomorphies
  • Rudixylon (Petriellales) Provides Clues on the Paleophysiology of a Triassic Polar Forest Shrub
  • SEPALLATA Gene Expression, WGDs, and Neofunctionalization in the Monocot Floral Tool Kit
  • Stomatal Guard Cell Size as Proxy for Paleopolyploidy in Vascular Plants Including Angiosperms
  • Support for a Gnepine Hypothesis Builds & Flowering Plants Are the Sister Group of Gymnosperms
  • Yale University Research on the Triassic Origin of Flowering Plants

  • REVISED AND POSTED ON AUGUST 1, 2016


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