[ The Big Picture ]
Certain students of the biology of extant basal flowering plants and magnoliids are so diligent and focused they become oblivious to paleobiological principles and neglect classical ideas published in the literature prior to the invention of The Internet and world-wide web.
Perhaps this is why some authors of scientific books and reviews of the vast literature on the origin of flowering plants and evolution of seed plants restate or revive classic works by Florin , Takhtajan , Axelrod , or Mamay's pivotal but neglected 1976 USGS Special Paper on the Paleozoic Origin of Cycads (Endress 2001, T. N. Taylor et al. 2009, Friis et al. 2011). According to Tomlinson (2012), the late Robert Brown, F.R.S., F.L.S., was one of these scientific giants (Figure 1 on page 311, Tomlinson 2012).
Solitary, angio-ovuliferous carpels of the "primitive" magnoliid tree, Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnolianae), are shown on either side of the text, above. The left image is a scanning electron micrograph of a portion of the stigmatic secretion of a carpel. A tiny, thread-like pollen tube emanates from a single boat-shaped monosulcate pollen grain, which is just visible on the left-hand surface of the secretory plug. The pollen grain adheres to the secretory surface, ×30. The right hand image is a cutaway view of angio-ovuly with cellular details of the carpel, placenta, ovules, and the stigmatic secretion, ×15.
"Gymno-ovuly is the original condition from which angio-ovuly must have evolved. Thus, the search for the origin of flowering plants must have an appreciation for the biological changes that have resulted in the shift of pollination of 'naked' ovules from that of 'enclosed' ovules ... " (page 312, Introduction - The flowering plants, Tomlinson 2012).
Pollen tubes probably penetrate the flared stigmatic secretion and might be attracted and/or guided to the egg of a modular female gametophyte inside one of several ovules enclosed by the carpel. Pollination and fertilization of degenerias has not been well-studied.
Both samples were field fixed in 1986 and later dissected from a flower collected in the canopy of a tagged and vouchered specimen of Degeneria vitiensis, Naitaradamu Study Area, Viti Levu, Fiji. The scanning electron micrographs were prepared by Al Soeldner, Director, Oregon State University Electron Microscopy Laboratory. I thank the National Geographic Society for funding for this field study.
Degeneria vitiensis was photographed by Paddy Ryan, Ph.D. in his 1986 kodachrome of a flower to the left. I thank Dr. Ryan for providing this image.
Let's not forget that 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 (Carlquist 1974, Morat et al. 2012).
Potential plastid genome conflict resulting from horizontal transfer (HT) of mitochondrial DNA (mtDNA) from parasitic santalalean flowering plants to Amborella trichopoda (Rice et al. 2013) should be explored.
Studies of HT in basal flowering plants by the Jeffrey Palmer Lab of Cornell University beg several questions.
What was the source paleopopulation of parasitic mistletoes (Santalales comprise 2200 species in 160 genera and 18 families, Nickrent et al. 2010) providing the invasive and exotic plastid DNA, which was incorporated into clonal tissues of Amborella trichopoda?
When in the nucleic acid history of Amborella trichopoda plastids did HT of cpDNA and/or mtDNA from a superasterid parasitic flowering plant population occur?
Could santalalean plastid DNA markers be used to identify the continental source of Amborella clones (and/or pinpoint the origin of bird-dispersed fruits containing captured plastid DNA) that colonized the island of New Caledonia (Nouvelle-Calédonie) during Paleogene tectonic and volcanic events (Figure 2.3 on page 18, and Table 2.1 on pages 26-27, Kroenke 1984, Morat et al. 2012)? Possibly.
Where among hundreds of candidate parasitic angiosperm sources could students of cpDNA and mtDNA HT initiate a search for molecular markers needed to track potential trajectories of Amborella stem- and root-mats from continental riverine sources (paleorivers) to the Loyalty Island Archipelago (Figure 1, Morat et al. 2012) of the South Pacific Ocean?
The largest river of the high islands of the South Pacific Ocean is the mighty Rewa of Viti Levu, Fiji, which is several hundred kilometers east of New Caledonia. Further, basement rocks of the Fiji Platform, d'Entrecasteau-, Loyalty-, and Norfolk ridges, are demonstrably ancient (Morat et al. 2012). Despite high endemism, vascular plants of New Caledonia colonized ancient, submerged basement rocks relatively recently, probably during the Oligocene Epoch (Morat et al. 2012), or much later in the Cenozoic.
Southeast asian populations of one or more species spread among 14 genera of Loranthaceae Tribe Elytrantheae, Tupeia antarctica, comprising monotypic Tribe Tupeinae (page 546, Nickrent et al. 2010), or a couple Malesian species in one or more subtribes of Lorantheae (page 548, Nickrent et al. 2010), might be places to start the search for a possible donor of plastid DNA to Amborella trichopoda. Students of parasitic flowering plants might also scan the indigenous New Caledonia population of Daenikera corallina (Vidal-Russell and Nickrent 2008), or related species (Table 1, op. cit.), as potential donor[s] of foreign circular DNA snippets in plastid genomes of amborellas.
"While the recolonisation of New Caledonia dates back only to the Oligocene, by long distance dispersal, many families belong to the ancient Gondwanan stock. This is notably the case for ... Amborellaceae, whose sole species globally (Amborella trichopoda) comprises the entire order Amborellales and is sister to all modern flowering plants (P. S. Soltis et al. 1999), although not their ancestor, as is often incorrectly indicated" (page 198, Analysis of the Various Vascular Plant Groups Represented in the Flora, Angiosperms, Dicotyledons, Richness and Composition, Morat et al. 2012).
Misodendraceae of the order Santalales probably first appeared in aerial canopies of Cretaceous forests some 80 MYA (Vidal-Russell and Nickrent 2008). Calibrated lamid phylogenies computed by Tripp and McDade (2014) suggest an older origin of asterids, probably during the Triassic or Jurassic periods.
Discussion. Implications of HT from an extinct population of superasterid parasitic flowering plants to cpDNA and mtDNA of Amborella trichopoda are curious and potentially troubling. Why?
Because the same research laboratory stated incorrectly in the first sentence of Chanderbali et al. (2016), a Jurassic or Cretaceous origin of the flower.
Based on fossil-calibrated phylogenomic analyses by C. S. P. Foster et al. (2017) and principles of stratigraphy is the statement by Chanderbali et al. (2016) on the first page of their paper accurate or precise?
"The origin of the flower during the late Jurassic to early Cretaceous eras was a key evolutionary innovation ..."
In my opinion, "assembly" (page 816, J. A. Doyle 2008) of perianth parts, microsporophylls, and megasporophylls to form a flower was an improbable and unnecessarily complicated saltational event punctuating a long and gradual evolutionary history of angiosperms. Flowering plants did not appear "suddenly," and sophomorical concepts of a so-called "first flower" should be rejected, in my opinion.
When in geologic history did angio-ovuliferous cone or floral organs first evolve? Probably during the Permian Period or earlier in the Paleozoic Era, based on extreme conservation of the floral tool kit.
The Amborella Genome Project adopts a curious phrase, "throughout angiosperm history," which was first coined by Zuccolo et al. (page 3, 2011), and suggests an asymptotic age for the origin of the Amborellanae clade "≈200 MYA," which is the approximate date of the end-Triassic mass extinction (PTr).
"The Amborella genome is a pivotal reference for understanding genome and gene family evolution throughout angiosperm history. Genome structure and phylogenomic analyses (Chamala et al. 2013) 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).
In my opinion, studies of the Amborella trichopoda genome are not pivotal despite the optimistic appraisal quoted, above.
Charles S. P. Foster et al. (2017) conclude that, "using analyses of near-complete chloroplast genomes, we have estimated that crown group Angiospermae arose 221 Ma (251-192 Ma) in the mid-Triassic."
Taking into account caveats raised by Harvard Professor Barry Tomlinson (2012), accomplished findings of The Amborella Genome Project team should have been cast in terms of the evolution of angio-ovulifery rather than invoking "angiosperm history," which remains an unsolved paleobiological mystery, probably involving allopolyploidy.
"Gene duplication is also a source of developmental innovation, but it is possible that it is not the increased number of genes (and their subsequent divergence) that is important in the evolution of new morphologies; rather it may be the increased number of regulatory regions that result from gene duplication which provides the raw material for morphological innovation ... " (page 338, Conclusions, Shubin and Marshall 2000).
Tool kit studies of the Amborella trichopoda genome probably do not offer a solution to angiosperm origins, but may provide critical insight on rewiring of gene-regulatory networks (GRNs) and auxin-based polarity networks (PINs), expressed as evo-devo in Permo-carboniferous seed plant lineages. Based on paleobiological principles (Shubin and Marshall 2000) genomic analyses may provide insight on the origins of evolutionary novelty but do not solve the origin of major eukaryotic clades, whether algal, animal, fungal, plant, or protist.
Based on the mechanism of allopolyploidy, and unsolvable paleobiological problems in pin-pointing zones of sympatry in hybridizing seed plant populations, the origin of flowering plants is a conundrum.
Amborella Genome Project. 2013. The Amborella genome and the evolution of flowering plants. Science 342(6165): 1467.
Axelrod, D. I. 1970. Mesozoic paleogeography and early angiosperm history. Botanical Review 36(3): 277-319.
Carlquist, S. 1974. Adaptive Radiation: New Caledonia and New Zealand. Pp. 214-252 in: Island Biology. New York: Columbia, 660 pp.
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.
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.
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.
Doyle, J. A. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169(7): 816-843.
Endress, P. K. 2001. Chapter 21. Origins of flower morphology. Pp. 493-510 In: G. P. Wagner (ed.), The Character Concept in Evolutionary Biology, San Diego: Academic Press, 622 pp.
Florin, R. 1954. The female reproductive organs of conifers and taxads. Biological Reviews 29: 367-389.
Foster, C. S. P., H. Sauquet, M. Van Der Merwe, H. McPherson, M. Rossetto, and S. Y. W. Ho. 2017. Evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale. Systematic Biology 66(3): 338-351.
Friis, E. M., P. R. Crane, and K. R. Pedersen. 2011. Early Flowers and Angiosperm Evolution. Cambridge: Cambridge University Press, 596 pp.
Kroenke, L. W. 1984. Chapter 2. New Caledonia: the Norfolk and Loyalty ridges; the New Caledonia and Loyalty basins. Pp. 15-28 In: L. W. Kroenke, Cenozoic Tectonic Development of the Southwest Pacific. United Nations ESCAP, CCOP/SOPAC Technical Bulletin No. 6, 122 pp.
Mamay, S. H. 1976. Paleozoic Origin of the Cycads. U. S. Geological Survey Professional Paper 934, 48 pp.
Morat, P., T. Jaffré, F. Tronchet, J. Munzinger, Y. Pellon, J-M. Veillon, M. Chalopin, F. Birnbaum, F. Rigault, G. Dagostini, J. Tinel, and P. P. Lowry II. 2012. Le référentiel taxonomique Florical et les charactéristiques de la flore vasculaire indigè de la Nouvelle-Calédonie. Adansonia 34(2): 179-221.
Nickrent, D. L., V. Malécot, R. Vidal-Russell, and J. P. Der. 2010. A revised classification of Santalales. Taxon 59(2): 538-558.
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.
Shubin, N. and C. R. Marshall. 2000. Fossils, genes, and the origins of novelty. Paleobiology 26: 324-340.
Soltis, P. S., D. E. Soltis, and M. W. Chase. 1999. Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature: 402: 402-404.
Takhtajan, A. 1969. Flowering Plants: Origin and Dispersal (translated by C. Jeffrey). Edinburgh: Oliver and Boyd, 310 pp.
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 pp.
Tomlinson, P. B. 2012. Rescuing Robert Brown - the origins of angio-ovuly in the seed cones of conifers. The Botanical Review 78: 310-334.
Tripp, E. A. and L. A. McDade. 2014. A rich fossil record yields calibrated phylogeny for Acanthaceae (Lamiales) and evidence for marked biases in timing and directionality of intercontinental disjunctions. Systematic Biology 63(5): 660-684.
Vidal-Russell, R. and D. L. Nickrent. 2008. The first mistletoes: origins of aerial parasitism in Santalales. Molecular Phylogenetics and Evolution 47(2): 523-537.
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.
"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 photograph on the left shows volcanic ash and tuff deposits of the Paleogene John Day Formation of western North America.
The right-hand image is the mouth of Santa Elena Canyon, which is a chasm carved by the Rio Bravo del Norte (Rio Grande) of southwestern North America. The massive exposure of sedimentary beds consists of several hundred meters of Lower Cretaceous Santa Elena Limestone. A sunlit portion of the cliff is part of Chihuahua, Mexico.
Creosote bush (Larrea tridentata, Zygophyllaceae, Zygophyllales, Rosanae) and ocotillo plants (Fouquieria splendens, Fouquieriaceae, Ericales, Asteranae) are visible in the foreground.