"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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[ Publication of the Year ]

Each year I will select a scientific paper, book chapter, or book as being of paramount importance toward solving the enigmatic origin of angiosperms (flowering plants) and understanding the paleobiology of interacting holometabolous insects including phytophagy, pollenivory, and coevolution of arthropod- and seed plant- developmental tool kits and body plans.

Spectacular outcrops and eroded monoliths of the 40 million-year-old petroliferous Eocene Sespe Formation are composed of purplish sandstone rock exposures visible in the right-hand image. Rounded cobbles, lenticular gravels, and water-worn pebbles and sands of these graded deposits, probably owe their shapes to scouring from the Colorado Paleoriver. The Sespe Sandstone Block of the Topatopa Mountains is uplifted by tectonic forces, and supports a relictual fabid and pinid population.

Based on the published record, which is available from the shelves of the Earth Science and Koshland Biological Science libraries of The University of California, Berkeley, and by accessing institutional subscriptions to scientific journals, serials, and books online, and by computer-aided searching of the literature, the outstanding scientific paper read on the origin of flowering plants and paleobiology of interacting Holometabola, is discussed below.

The Outstanding Scientific Paper of 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 below) 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.

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. 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.

Floyd, S. K. and J. L. Bowman. 2007. The ancestral developmental tool kit of land plants. International Journal of Plant Sciences 168(1): 1-35.

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.

Hufford, L. 1997. The roles of ontogenetic evolution in the origins of floral homoplasies. International Journal of Plant Sciences 158: S65-S80.

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.



Previous Publication of the Year:

Best of year 2014. Proceedings of the 17th Evolutionary Biology Meeting at Marseilles, France are reported in a book, Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life, which is edited by Pierre Pontarotti. Chapter 13 of the proceedings is authored by Conrad Labandeira, a Smithsonian Institution Department of Paleobiology entomologist. The book chapter by Conrad Labandeira is the outstanding scientific paper of 2014, in my opinion.

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.

Conrad Labandeira provides a painstaking analysis of a new data set on family-level asynchronous co-radiations of angiosperms with the families belonging to the holometabolous "Big Five" insect orders of pollinivores and pollinators (including Triassic Obrieniidae and Tipulidae) plus Triassic Pseudopolycentropodidae (Mecoptera), Trichoptera, and protohymenopteran Xyelidae, and new data on phytophagous families of hemimetabolous Paraneoptera and Polyneoptera (Table 13.1 on pages 265-271, 2014).

The book chapter by Labandeira (2014) contains these key findings:

  • (1) "The angiosperm radiation ... One of the major episodes in the evolution of insect herbivory is the transition from gymnosperm to angiosperm-hosts during the initial diversification of angiosperms 125 to 90 million years ago"
  • (2) "The pattern ... Thus, a major [Aptian-Albian, page 288, Figure 13.3] gap occurred during these two [angiosperm-gymnosperm host-associated insect families] diversity maxima levels present on both sides of the angiosperm radiation ... " [attributable to "major turnover and time-lag effects"]
  • (3) "Implications ... The ecology of interactions between these older insect lineages and their dominantly gymnosperm hosts needs to be explored further [see also Labandeira et al. 1994] to establish an entrée into this earlier world devoid of angiosperms"
  • Is the early Cretaceous Period the interval in geologic time when the "initial diversification of angiosperms" occurred, if palynological data are considered? No, according to Hochuli and Feist-Burkhardt (2013).

    Further, 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), does not obviate a coevolutionary origin and "early radiation" of paraphyletic stem-group angiosperms with certain lineages of Permo-carboniferous Holometabola.

    "We have, however, considerable potential bias in the fossil record" (page 130, A. C. Scott et al. 1992).

    A discussion of a detailed study of pollen samples recovered from isolated sedimentary layers in [at least one] continuous stratigraphic sequence in two deep well cores, reports monosulcate, columellate palynomorphs, and Afropollis, from the Middle Triassic (Anisian) about 240 MYA (Hochuli and Feist-Burkhardt 2013) is not included by Labandeira (2014). This is understandable when drafting a chapter of a book volume authored by many scientists following peer-review and scheduling deadlines.

    Would Afropollis and other pollen morphologies found by Hochuli and Feist-Burkhardt (2013) be found in the preserved guts of [as yet undiscovered] Triassic insects? At least Afropollis and some angiosperm-like pollen morphotypes are found in arthropod guts fossilized in younger rocks (page 355 in Dmitriev and Ponomarenko 2002, Krassilov et al. 2003, among others).

    Students of a Triassic origin of angiosperms and the paleopalynology of Afropollis should read two reviews by Doyle et al. (1990 [see page 1549]). 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 the Neocomian (mid-Hauterivian) origin of flowering plants proposed by Friis et al. (2011), among others.

    Further, arguments posed by J. A. Doyle and Endress (2014) on evolution of Afropollis and evo-devo of pollen nexine to counter findings by Hochuli and Feist-Burkhardt (2013) should not be taken seriously, in my opinion.

    Analysis of 280 data entries on pages 265 through 271 of Table 13.1 (Labandeira 2014) and discussion of macroecological- and evolutionary patterns emerging from these data (Figures 13.2 and 13.3, Tables 13.2 and 13.3) provides rigorous proof of earlier work (Labandeira and Sepkoski 1993, Gómez-Zurita et al. 2007, among others). Some paleobotanists were uncomfortable with Labandeira and Sepkoski's conclusions, which was counter-intuitive to coevolutionary thinking in some halls of paleoentomology.

    Coevolution of stem group flowering plants and certain lineages of holometabolous insects is probably difficult, if not impossible, to prove in paleopopulations. But evo-devo is not, when considering ancient LTR-retrotransposon-mediated modification of genomic ["island"] landscapes (Civáň et al. 2011, among others) and horizontal [and vertical] transfer (Lovisolo et al. 2003, Tu 2005, Aravin et al. 2007, de la Chaux and A. Wagner 2011, among others), paleontologic evidence of highly conserved auxin polarity networks (Rothwell et al. 2014, among others), and molecular-phylogenetic analysis of DNA-binding tool kit enzymes including homeodomain proteins, PINs, and TFs (see discussion of a previous publication of the year, below).

    Surprisingly, Labandeira's findings (2014) might also help disprove the notion of a Hauterivian (Lower Cretaceous) origin of flowering plants (Hughes 1994, Friis et al. 2013), which is strangely incongruent with the stratigraphic distribution of Afropollis throughout the Mesozoic, because coevolution of insects and flowers is unsupported by macroecological data in a 35 million year interval in geologic time from Barremian to Turonian.

    "Angiosperms certainly contributed to the spectacular diversity of beetles, but these insects were well on their way at least 100 million years before angiosperms came on the scene ... "

    The preceding statement is quoted from page 399 of David Grimaldi and Michael S. Engel (2005), Evolution of the Insects. Cambridge: Cambridge University Press, 755 pp.

    Was Triassic Pangaea a "world devoid of angiosperms" (page 295, Conclusions, Labandeira 2014). No, according to Cornet (1986, 1989, 1993), Zavada (2007), and Hochuli and Feist-Burkhardt (2013).

    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. Curiously, citation and discussion of Labandeira's 2014 book chapter is somehow overlooked by most of the contributors to this volume.

    Late Paleozoic phytophagous insect lineages. One possible next step in a macroevolutionary study of the third phase of "insect expansions in deep-time" (Labandeira 2006), is to trace certain clades of Holometabola across the PTr boundary, and to compare these data with a detailed paleobotanical study of Permian delnorteas, evolsonias, and Vojnovskyales (and their congeners) as insect mutualists and seed plant hosts were dispersed to the early Triassic hothouse.

    "It should be stressed that even if there were some Palaeozoic insect pollinated plants their pollination systems were probably completely destroyed in the course of the Late Permian extinction that would have seriously affected all insect taxa that were biologically connected with plant reproductive organs."

    The preceding statement is quoted from page 355 of V. Yu. Dmitriev and A. G. Ponomarenko, (2002), 3. General features of insect history, Pp. 325-435 In: A. P. Rasnitsyn and D. I. J. Quicke (eds.), History of Insects. London: Kluwer Academic Publishers, 517 pp.

    According to Grimaldi and Engel (page 469, Figure 12.1, 2005) Panorpida, which are a sister group to the Hymenoptera (ants, bees, and wasps), diverged more than 290 MYA, roughly coincident with the angiosperm-gymnosperm split. Did protohymenopterans including sawflies (xyelids) possess mushroom bodies, optic lobes, and sensory tool kits necessary to visualize pigments of foliar organs, including protoflowers? Studies from the Chittka and Strausfeld labs (Chittka et al. 1994, Chittka 1996, Strausfeld et al. 1998, Briscoe and Chittka 2001, Chittka et al. 2001, Strausfeld 2009, X. Ma et al. 2012) may provide clues.

    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 in "sensory color space" (page 846, The use of floral morphospaces in evolutionary ecology: the sensory color space, Chartier et al. 2014)?

    "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).

    There are several reviews on the subject of insect interactions with late Paleozoic and early Mesozoic vascular plants, with extensive bibliographies (Béthoux 2009, Béthoux et al. 2005, Dmitriev and Ponomarenko 2002, Grimaldi and Engel 2005, Labandeira 1998, 2006, Scott et al. 1992, among others).

    Bibliography:

    Aravin, A. A., G. J. Hannon, and J. Brennecke. 2007. The piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764.

    Béthoux, O. 2009. The earliest beetle identified. Journal of Paleontology 83(6): 931-937.

    Béthoux, O., F. Papier, and A. Nel. 2005. The Triassic radiation of the entomofauna. Comptes Rendus Palevol 4: 609-621.

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

    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.

    de la Chaux, N. and A. Wagner. 2011. BEL/Pao retrotransposons in metazooan genomes. BMC Evolutionary Biology 11: 154.

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

    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.

    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.

    Civáň, P., M. Švec, and P. Hauptvogel. 2011. On the coevolution of transposable elements and plant genomes. Journal of Botany (Hindawi) 2011: 893546.

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

    Dmitriev, V. Yu. and A. G. Ponomarenko. 2002. 3. General features of insect history, Pp. 325-435 In: A. P. Rasnitsyn & D. I. J. Quicke (eds.), History of Insects. London: Kluwer Academic Publishers, 517 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).

    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.

    Gómez-Zurita, J., T. Hunt, F. Kopliku, and A. P. Vogler. 2007. Recalibrated tree of leaf beetles (Chrysomelidae) indicates independent diversification of angiosperms and their insect herbivores. PLoS ONE 2(4): e360.

    Grimaldi, D. and M. S. Engel. 2005. Evolution of the Insects. Cambridge: Cambridge University Press, 755 pp.

    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.

    Hughes, N. F. 1994. The Enigma of Angiosperm Origins. Cambridge: Cambridge University Press, 303 pp.

    Krassilov, V., M. Tekleva, N. Meyer-Melikyan, and A. Rasnitsyn. 2003. New pollen morphotype from gut compression of a Cretaceous insect, and its bearing on palynomorphological evolution and palaeoecology. Cretaceous Research 24: 149-156.

    Labandeira, C. C. 1998. Early history of arthropod and vascular plant associations. Annual Review of Ecology and Planetary Sciences 26: 329-377.

    Labandeira, C. C. 2006. The four phases of plant-arthropod associations in deep time. Geologica Acta 4(4): 409-438.

    Labandeira, C. C., D. L. Dilcher, D. R. Davis, and D. L. Wagner. 1994. Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution. Proceedings of the National Academy of Sciences 91(25): 12278-12282.

    Labandeira, C. C. and J. J. Sepkoski, Jr. 1993. Insect diversity in the fossil record. Science 261: 310-315.

    Lovisolo, O., R. Hull, and O. Rösler. 2003. Coevolution of viruses with hosts and vectors and possible paleontology. Pp. 325-379 In: K. Maramorosch, F. A. Murphy, and A. J. Shatkin (eds.), Advances in Virus Research, Volume 62. Boston: Elsevier-Academic Press.

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

    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.

    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.

    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.

    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.

    Scott, A. C., J. Stephenson, and W. C. Chaloner. 1992. Interaction and coevolution of plants and arthropods during the Paleozoic and Mesozoic. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 335: 129-165.

    Strausfeld, N. J. 2009. Brain organization and the origin of insects: an assessment. Proceedings of the Royal Society of London, Series B, Biological Sciences 276(1664): 1929-1937.

    Strausfeld, N. J., L. Hansen, Y. Li, R. S. Gomez, and K. Ito. 1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learning and Memory 5(1): 11-37.

    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.

    Tu, Z. 2005. 4.12. Insect transposable elements. Pp. 395-436 In: L. I. Gilbert, K. Iatrou, and S. S. Gill (eds.), Comprehensive Molecular Insect Science, Volume 4, Biochemistry and Molecular Biology. Amsterdam: Elsevier, 3200 pp.

    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.

    Notes added after-the-fact. Paleobiological studies of the Cretaceous entomofauna continue (Arens and Gleason 2016). Evidence of leaf feeding in the Soap Wash Flora, specifically in generalized foliar damage, supports the idea of an "Albian-Aptian gap" (see bulleted item No. 2, above), which is also discussed on page 288, Figure 13.3 of Labandeira (2014).

    The scanning electron micrograph shown to the right is the anterior exoskeleton of Haptoncus tahktajanii (Nitidulidae, Coleoptera), the cucujiform phytophagous associate of the primitive magnoliid flowering plant Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnolianae). Some of the gustatory, olfactory, and visual sensory organs of the nitidulid beetle are visible including antennae, sensillae, compound eyes, mandibles, maxillae, and labia.

    Arens, N. C. and J. P. Gleason. 2016. Insect folivory in an angiosperm-dominated flora from the mid-Cretaceous of Utah, U.S.A. Palaios 31: 71-80.

    Best of year 2013. Four significant conclusions from a study of molecular phylogenies of the WUSCHEL family of homeodomain proteins and the WOX homeobox shed light on stem cell niches and vegetative leaf morphologies of the last common ancestor of angiosperms and gymnosperms. Phylogenies were computed from inferred amino acid sequences of the DNA-binding homeodomain by genome walking of the WUSCHEL and WUS/WOX5 homeobox genes by plant biologists from the Institute of Developmental Biology, University of Cologne:

    Nardmann, J. and W. Werr. 2013. Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches. New Phytologist 199(4): 1081-1092.

    Critically important research by Nardmann and Werr (2013) discussing eudicot and Gnetum foliar tool kit process homology and deeply conserved angiosperm and gymnosperm shoot apical meristem (SAM) transcription factors (TFs), is a clear choice for outstanding publication of the year. An earlier installment of this work is relevant:

    Nardmann, J., P. Reisewitz, and W. Werr. 2009. Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Molecular Biology and Evolution 26(8): 1745-1755.

    Angiosperms are sister to Gnetales, Ginkgo, cycads, Pinaceae, and Cupressaceae in Figure 5 (Nardmann and Werr 2013). Expression patterns, and a WOX cladistic analysis, suggesting eudicot and Gnetum process homology, were not calibrated by late Paleozoic fossils (Discussion, Nardmann and Werr 2013).

    Yet, Permian Gnetum-like seed plant permineralized leaves have been anatomically studied by Mamay et al. (1988), and venation patterns of these Leonardian fossils are identical to Figure 5a on page 1088 (Nardmann and Werr 2013) and Figure 3 on page 346 ("character 5-7" ["110"] in text, J. A. Doyle and Donoghue 1986).

    "We also placed leaves of angiosperms and Gnetum in the 110 category, since their derivation from taeniopteroid ancestors would involve no change in major venation, only origin of reticulations and interpolation of new vein orders [coded as characters 9 and 10], whereas derivation from pinnately compound would require at least one additional step, simplification" (page 347, J. A. Doyle and Donoghue 1986).

    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.

    Notes added after-the-fact. Fascinating insight from biochemical research of WUSCHEL homeodomain protein TFs and the foliar tool kit, including knockout studies of the WOX homeobox, continue to surface in the literature (J. M. Alvarez et al. 2015). This line of research might help us in disentangling evolutionary-development of the MRCA and deciphering whole plant morphologies seen in developmental fingerprints of detached and shed Paleozoic seed plant foliar fragments.

    Alvarez, J. M., J. Sohlberg, P. Engström, Tianqing Zhu, M. Englund, P. N. Moschou, and S. von Arnold. 2015. The WUSCHEL-RELATED HOMEOBOX 3 gene PaWOX3 regulates lateral organ formation in Norway spruce. New Phytologist 208(4): 1078–1088.

    "The similarities in expression patterns in needle primordia between PaWOX3 and its orthologues in the gymnosperms Ginkgo biloba, Gnetum gnemon and Pinus sylvestris (Nardmann and Werr, 2013), suggest that the expression pattern and functions of PaWOX3-related genes might be shared between all gymnosperms."

    This work illuminates details of a "largely conserved" process homology among foliar tool kits of cycads, ginkgos, gnetophytes, malvids, and pinids.

    "Thus, the phenotypic consequences of PaWOX3 knockdown in Norway spruce resemble those observed in mutants for the orthologous genes in angiosperms. Both in Norway spruce and angiosperm models, needles/leaves and cotyledons are narrower and curled or folded, and lateral margin development is impaired, indicating that WOX3 is instrumental for lateral margin cell growth and development."

    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. nov. ["the probable cycadophyte" cited and discussed on another page]) 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 phenotypes of developmental regulation visible in detached and shed Permian seed plant leaf fossils, was the foliar tool kit of delnorteas, evolsonias, and retuse taeniopteroids underpinned by the same WOX homeobox genes, WUSCHEL homeodomain proteins, and CUC2 TFs as extant model flowering plant species?

    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 gigantopteroid and taeniopteroid leaves, representing hybridizing seed plant populations at the base of the angiosperm stem.

    Are angiosperm-like lignophytes the backbone of Upper Paleozoic seed plant lineages? Yes, from the research perspective of the deeply conserved foliar and floral short- [spur-] shoot tool kit and from molecular-phylogenetic studies of phytochrome genes encoding their deeply-conserved protein amino acid sequences (Mathews and Donoghue 1999).

    By reviewing the vast literature on tool kit evo-devo, and through incorporation of molecular-phylogenetic studies by Beaulieu, Chase, Donoghue, Mathews, Savard, and Stephen A. Smith, among others, coupled with modeling of the alpha (α)- swarm of WGDs by Jiao and colleagues, I have reached a surprising conclusion that intergeneric hybrids between Permo-carboniferous gigantopteroids including Delnortea abbottiae and Evolsonia texana, and species of Vojnovskyales constitute the allopolyploid ancestors of angiosperms.

    Bibliography:

    Aravind, L., V. Anantharaman, S. Balaji, M. M. Babu, and L. M. Iyer. 2005. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiology Reviews 29: 231-262.

    Bharathan, G., T. E. Goliber, C. Moore, S. Kessler, T. Pham, and N. R. Sinha. 2002. Homologies in leaf form inferred from KNOX1 gene expression during development. Science 296: 1858-1860.

    Bharathan, G., B.-J. Janssen, E. A. Kellogg, and N. R. Sinha. 1997. Did homeodomain proteins duplicate before the origin of angiosperms, fungi, and metazoa? Proceedings of the National Academy of Sciences 94(25): 13749-13753.

    Bharathan, G., B.-J. Janssen, E. A. Kellogg, and N. R. Sinha. 1999. Phylogenetic relationships and evolution of the KNOTTED class of plant homeodomain proteins. Molecular Biology and Evolution 16(4): 553-563.

    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.

    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.

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

    Mathews, S. and M. J. Donoghue. 1999. The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286: 947-950.

    Savard, L., P. Li, S. H. Strauss, M. W. Chase, M. Michaud, and J. Bousquet. 1994. Chloroplast and nuclear gene sequences indicate late Pennsylvanian time for the last common ancestor of extant seed plants. Proceedings of the National Academy of Sciences 91(11): 5163-5167.

    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.

    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.



    Archived Publication of Year's Previous:

    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.

    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.

    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.

    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.

    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.

    The right-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.

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

    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 Publishing Ltd., 304 pp.

    Soltis, D. E., P. S. Soltis, P. K. Endress, and M. W. Chase. 2005. Phylogeny and Evolution of Angiosperms. Sunderland: Sinauer, 370 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.


    The North American Transverse Ranges including a detached and uplifted block of the petroliferous Eocene Sespe Formation, support populations of silvery false-lupine. The population of Thermopsis californica var. argentata (Fabaceae, Fabales, Rosanae) indigenous to the rugged Sespe Region, is of interest to students of biogeography, botany, ecology, and systematics. One of the Bear Heaven clones pictured below, is growing on soil derived from weathered Sespe Sandstone.

    Sandstone cliffs have kept the incidence of catastrophic wildfire to a minimum allowing three species of pinids to survive on ledges and crevices of charismatic bluffs and eroded monoliths north of Santa Paula Peak, shown above and southwest of Bear Heaven. Abies concolor (white fir), Pinus lambertiana (sugar pine), and Pseudotsuga macrocarpa (big cone Douglas fir) constitute the indigenous coniferous population of the Sespe Sandstone Block of the Topatopa Mountains.

    The images on this page were captured by the author in 1970 using Kodak ASA 25 film as part of a biome project conducted by S. Allen Cattel, Richard May, John M. Miller, and Bernie Rios for a Moorpark College biology class taught by the late Clinton Schoenberger. Two of these community college students (Cattel and Miller) went on to earn their doctorate degrees from The University of British Columbia and Oregon State University, respectively.

    Twenty-five years later a team of biologists led by Richard Burgess documented the Bear Heaven population of silvery false-lupine in the relict conifer stand shown above. I thank Dieter Wilken, Ph.D. of the Santa Barbara Botanical Garden for bringing the Burgess museum specimen of Thermopsis californica var. argentata (SBBG 123477) to my attention.


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    LIST OF RESOURCES

  • Library and Classroom Resources
  • Primer on Developmental Tool Kits
  • Publication of the Year
  • Reading List of Books and Book Chapters
  • The Charles Darwin Bicentennial Reading List
  • Topics for Class and Seminar Debate and Discussion
  • Student Problems
  • A Problem in Paleobotany, Taphonomy, and Computing Theoretical Morphospace
  • Drill in Magnoliid Pollen Phylogenetics
  • Exercise in ARC-INFO/GIS, Geo-referencing, and Paleobiogeography

  • THIS PAGE WAS UPDATED ON JUNE 1, 2016


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