A flowering branch of Sphaeralcea emoryi (Malvaceae, Malvales, Rosanae) is pictured to the right. Sphaeralceas are common wildflowers of North American deserts, grasslands, woodlands, and lower slopes of arid mountains.
Amborella Genome Project:
Produced by Professor C. W. dePamphilis and colleagues this United States National Science Foundation sponsored web site, which is hosted by The Pennsylvania State University, focuses on a landscape of the pivotal Amborella trichopoda (Amborellaceae, Amborellales, Amborellanae) genome ... LINK
Arboretum de Villardebelle:
What a great site to discover the biology and diversity of gymnosperms, among others! The Arboretum de Villardebelle is located in southwestern France ... LINK
Botanical Society of America's Carnivorous Plant Pages:
Students and the web-browsing public will enjoy this visit to insect Hell, sponsored by the Botanical Society of America that focuses on insect-eating plants. Learn how antagonism can follow a different path ... LINK
Cosmoss Dot Org:
The Physcomitrella bioinformatics and plant transcriptional factor (PlanTAFDB) data bases, and BLAST tool kits are accessible from the Physcomitrella patens resource web site ... LINK
Fairchild Tropical Botanical Garden:
The garden's mission is to "save tropical plant diversity by exploring, explaining and conserving the world of tropical plants; fundamental to this task is inspiring a greater knowledge and love for plants and gardening so that all can enjoy the beauty and bounty of the tropical world." This web site is a good resource for palms and Neotropical botany with an attractive "flash" graphic on its home page ... LINK
Floral Genome Project:
This site is an excellent learning tool for molecular plant systematists and Cenozoic paleobotanists which was funded by a grant from the United States National Science Foundation ... LINK
Carleton University hosts this student friendly educational web site that explores genomics as a tool in bettering our understanding of evolution ... LINK
Grassius Dot Org:
This is the official web site of developmental regulation for agrostologists who study cis-regulatory modules (elements) in grasses (Poaceae) ... LINK
Harvard University Herbaria:
Harvard University Herbaria Home Pages which contain an extensive nomenclatural database including the International Plant Names Index ... LINK
Missouri Botanical Garden's Database Server:
This site provides access to the Missouri Botanical Garden's VAST (VAScular Tropicos) nomenclatural database and associated authority files ... LINK
Monocot Dot Org:
This educational web site on aspects of monocotyledonous flowering plants is sponsored the British Natural Environment Research Council in a grant to the Royal Botanic Gardens, Kew and Natural History Museum of Oxford University ... LINK
MrBayes Web Page:
Need to apply Bayesian priors to your data set? A review by Ronquist et al. (2012) is available. Follow this link to the MrBayes Version 3.2 download page ... LINK
Planting Science Dot Org:
Developed and supported by The Botanical Society of America, this online learning resource connects students, teachers, and plant scientists across the United States of America. American students, from middle school to college level, engage in hands-on inquiry projects and share their experiences with peers and scientist mentors. Compiled by David Spooner, the web site is a good learning resource with several links to other URL's ... LINK
Professor William Burger's Website:
The Department of Botany of the Field Museum hosts this interesting discussion of Bill Burger's proposals on the origin of flowering plants, which is centered on a "Monocots-first-scenario" ... LINK
Professor Scott Russell's Website:
Scott's Links is a University of Oklahoma hosted web site, which is authored by Professor Scott Russell. The site contains links to library resources for students, teachers, and research botanists who need to find reliable information online ... LINK
Professor Peter Steven's Angiosperm Phylogeny Website:
Professor Peter F. Stevens under the auspices of the Missouri Botanical Garden has compiled this detailed library resource for use by students, teachers, and research botanists interested in phylogeny of flowering plants. The site, which is based on the Angiosperm Phylogeny Group's proposed classification of orders and families of flowering plants contains extensive data on morphological and biochemical characters complete with bibliographies, character sets, distribution maps, and sample cladograms. One feature of the phylogenetic reconstructions is built-in linkage with metadata ... LINK
Royal Botanic Gardens, Kew:
This is the official web site for the Kew Gardens ... LINK
The Laboratory for Molecular Systematics and Evolutionary Biology is featured by Professor Pamela S. Soltis and Douglas E. Soltis ... LINK
Students and teachers conversant in French will find cutting-edge classroom and laboratory resources having to do with introductory botany in the web page content of the Massive Open Online Course ... LINK
The New York Botanical Garden:
The New York Botanical Garden home page provides access to several databases including Index Herbariorum. The NYBG has one of the world's finest libraries on the origin of flowering plants, which was assembled by Rudolf Schmid, Ph.D., including a card index to books and reprints on the subject ... LINK
Tree of Life Project:
Originally designed for biologists this site has been adapted for use by students and teachers in high school and college to help them better understand the evolution of life on Earth. Gigantopteroid readers should be especially interested in section of the Tree of Life web site that deals with angiosperms and the fossil history of the group. Compiled by Christine Edwards, Doug Soltis, and Pam Soltis the page devoted to angiosperms is a good learning resource with several links to other web sites ... LINK
University of Calgary Algorithmic Botany Web Site:
Interested in modeling plant development and the mechanical forces of insect exoskeletons on plant cell surfaces? Check out this web site ... LINK
University of California, Berkeley Jepson Herbarium:
Students of California botany should add this link to their favorites. This is the portal to the University and Jepson Herbaria databases ... LINK
University of California Botanical Garden:
This is the gateway to one key Center for Plant Conservation, which is located in Strawberry Canyon on the campus of The University of California, Berkeley ... LINK
Calibrating Pollen Trees:
Students of magnoliid phylogenetics and the paleopalynology of Afropollis, Tucanopollis, and other pollen morphotype genera, should read several reviews on the evolution of angiosperm pollen before proceeding with the following drill (J. A. Doyle et al. 1990 [see page 1549], J. A. Doyle and Hotton 1991, J. A. Doyle 2005, 2009, Wortley et al. 2015).
To the right is a close-up snapshot of developing pollen borne in a furrow of a microsporophyll of Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnolianae) ×400, which resembles Hochuli and Feist-Burkhardt's Pollen Type 1.
The pollen-bearing organ was hand-collected from a flowering tree in the Naitaradamu stand on the island of Viti Levu, Fiji (J. M. Miller 1989). Al Soeldner of the Oregon State University Electron Microscope Laboratory prepared and imaged the sample. Field work on Degeneriaceae of the Fiji Islands was sponsored by a grant from the National Geographic Society.
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.
Student problem. 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.
As a practice drill in phylogenetics recompute the cladogram in Figure 2 on page 1562 of J. A. Doyle et al. (1990) to include Afropollis from the Middle Triassic (Hochuli and Feist-Burkhardt 2013).
Now choose an outgroup from a suite of Permo-triassic palynofloras including potential semaphoronts from Hochuli and Feist-Burkhardt (2004, 2013), and Zavialova and Gomankov (2009). After adding anatomical characters from studies of Albian pollen (Horikx et al. 2016), what can you conclude about the origin of magnoliids including Annonaceae, Chloranthaceae, Degeneriaceae, Himantandraceae, Lactoridaceae, and Winteraceae?
Do arguments published by J. A. Doyle and P. K. Endress (2014) on anomalous nexine sporopollenin thickness and the validity of Peter Hochuli and Susanne Feist-Burkhardt's paleopalynological data hold any water?
Probably not, according to the statement by C. S. P. Foster et al. in the second paragraph of their paper, which is published in Systematic Biology (page 338, 2017).
Based on fossil calibrations in the context of evolutionary rates and geologic time (Marshall 2008, Quental and Marshall 2010, J. A. Doyle 2015, Massoni et al. 2015), and taking into account the deeply conserved floral tool kit of short- (spur-) SAMs, what if anything, do Caytoniales have to do with the origin of the magnoliid clade?
Angiosperm pollen phylogenies might offer fuel for debate and discussion (Tripp and McDade 2014, L. Lu et al. 2015), but are your results congruent with phylogenetic analyses computed by J. A. Doyle (2015) and Massoni et al. (2015)?
Upon careful reading of James A. Doyle's three decade-long review and study of extant and fossil magnoliid pollen (J. A. Doyle 2015), discuss differences, if any, on the taxonomic placement and evolutionary history of Afropollis.
"... this paper will alert palynologists and paleobotanists working in the Gondwana continents to winteraceous pollen and megafossils, and thus contribute to a more detailed reconstruction of the history of this important family of primitive angiosperms ..." (Conclusions, page 313, J. A. Doyle 2000).
Hochuli and Feist-Burkhardt's discovery of magnoliid pollen in well logs of cores recovered in buried sediments from Triassic Pangaea has clouded the evolutionary history of the "earliest" flowering plants outlined by J. A. Doyle (2005, 2015), L. Lu et al. (2015), and APG IV (2016), among others. This begs several questions:
Do palynological data and past analyses by J. A. Doyle, E. M. Friis, J. Kvaček et al., L. Lu et al., and J. W. Walker (also see references listed below), among others, clear-up our understanding of the origin of the magnoliid clade including "D & E- or J/M-backbone" trees, which are discussed in the Introduction on page 416 of J. A. Doyle (2015) and on page 1360 of Kvaček et al. (2016)?
Several workers adopt the sophomoric view that angiosperm monophyly is unequivocal and/or "rooted" by Amborella trichopoda (L. Lu et al. 2015). These authors provide "evidence of plesiomorphic characters in pollen," yet marginalize Cornet, Habib, Hochuli and Feist-Burkhardt, and Zavada palynological data by ignoring several important papers that offer contradictory points of view.
"... The total number of phylogenetic lines established by the late Albian may be greater than might be expected based on their relatively uniform reticulate monosulcate and tricolpate pollen. However, similar plesiomorphic pollen types are widely distributed among modern 'basal' lines, and there are none of the glaring inconsistencies noted by early palynologists between old identifications of fossil leaves with modern taxa and the level of advancement of pollen types at the same horizons ..." (Conclusions, page 425, J. A. Doyle 2015).
Students now have an opportunity to re-do the J. A. Doyle, J. Kvaček et al., and L. Lu et al. morphological-phylogenetic pollen analyses with Hochuli and Feist-Burkhardt data by including "reticulate monosulcate plesiomorphic pollen types," now known from sedimentary rock layers Triassic in age.
Is the statement by J. A. Doyle quoted above, consistent with discussion published by Cornet (1989, 1993), Cornet and Habib (1992), and Zavada (2007)?
How do published pollen phylogenies of basal angiosperms and magnoliids change when palynological data on Jurassic and Triassic flowering plants are added to datasets?
Incorporating Anisian palynological data to calibrate pollen phylogenies, and accounting for intergeneric hybridization and allopolyploidy, could unravel APG IV.
"Using analyses of near-complete chloroplast genomes, we have estimated that crown-group Angiospermae arose 221 Ma (251-192 Ma), in the mid-Triassic. This inferred age is at least ≈50 myr, and up to ≈110 myr, older than the oldest known fossils attributed to crown-group angiosperms" (page 349, Conclusions, C. S. P. Foster et al. 2017).
A pivotal biochemical study of the sacred lotus genome by Yun Wang and coworkers (2013) reveals no trace of a "γ (gamma) triplication," which is a key marker in the evolutionary history of eudicots and monocots (Jiao et al. 2011, Jiao et al. 2012, P. S. Soltis and D. E. Soltis 2016). This study places Nelumbo nucifera as an [auto- or allo-?]tetraploid in a basalmost position among the crown group of extant eudicots.
Based on modeling studies of the "γ triplication" (Jiao et al. 2012), are angio-ovuliferous flowering plants as a whole, monophyletic or paraphyletic?
Concluding remarks. Some students of angiosperm systematics, paleoecology and physiology, and morphological-phylogenetics adopt decisive and conclusive terminology "earliest," "ancestral," "early," "early-divergent," "primitive," or "very early stage," when discussing Lower Cretaceous basal flowering plants and magnoliids sensu APG IV. In my opinion, persistent use of such modifiers is troubling.
"... A Cretaceous origin of the sunflower alliance is significant for timing flowering plant evolution in general (1), because the sunflower and bellflower families are among phylogenetically the most specialized of all flowering plants ... early angiosperm diversification may have been even older ..." (Discussion on page 9190, K. Bremer and M. H. G. Gustafsson 1997).
Paleobiologists should not forget that lamid palynomorphs referable to Acanthaceae are known from sediments Triassic in age (Tripp and McDade 2014). Further, Hochuli and Feist-Burkhardt data (2004, 2013) are unequivocal. Finally, certain paleoecologists and physiologists should pay attention to this statement:
"With both Nymphaea and Amborella at the base of the latest angiosperm tree, a wider range of characters might be expected in archetypical angiosperms or angiosperm sister groups than that implied by previous consensus on Amborella alone. What of complementary projections derived from analysis of seed plant relationships? Do these analyses point toward likely archetypal angiosperms or angiosperm ancestors? No. Not when we incorporate the recent analyses challenging the validity of the anthophytes. Instead, angiosperms become more distantly related to all existing seed plants, leaving a gap populated only by extinct taxa that may or may not be represented in the fossil record" (Crepet 2000).
The above quotation is from W. L. Crepet (2000), Progress in understanding angiosperm history, success, and relationships: Darwin's "abominably perplexing phenomenon," Proceedings of the National Academy of Sciences 97 (24): 12939-12941.
I conclude this student exercise on pollen cladistics with images of modern-day asterids and lamids (see below). Tom Daniel, Ph.D. is thanked for bringing the micropaleontological studies on lamid palynomorphs referable to Acanthaceae to my attention.
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.
Bremer, K. and M. H. G. Gustafsson. 1997. East Gondwana ancestry of the sunflower alliance of families. Proceedings of the National Academy of Sciences 94: 9188-9190.
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.
Couvreur, T. L. P., M. Botermans, B. J. van Heuven, R. W. J. M. van der Ham. 2008. Pollen morphology within the Monodora clade, a diverse group of five African Annonaceae genera. Grana 47(3): 185-210.
Doyle, J. A. 2000. Paleobotany, relationships, and geographic history of Winteraceae. Annals of the Missouri Botanical Garden 87(3): 303–316.
Doyle, J. A. 2005. Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses. Grana 44(4): 227-251.
Doyle, J. A. 2009. Evolutionary significance of granular exine structure in the light of phylogenetic analyses. Review of Palaeobotany and Palynology 156(1-2): 198-210.
Doyle, J. A. 2010. Function and evolution of saccate pollen. New Phytologist 188: 6-9.
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.
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. and C. L. Hotton. 1991. Diversification of early angiosperm pollen in a cladistic context. Pp. 169-195 In: S. Blackmore and S. H. Barnes (eds.), Pollen and Spores: Patterns of Diversification, The Systematics Association Special Volume no. 44. Oxford: Oxford University Press, 391 pp.
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.
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. 1997. Fossil history of magnoliid angiosperms. Pp. 121-156 In: K. Iwatsuki and P. H. Raven (eds.), Evolution and Diversification of Land Plants. Tokyo: Springer-Verlag, 330 pp.
Friis, E. M. and K. R. Pedersen. 2011. Canrightia resinifera gen. et sp. nov., a new extinct angiosperm with Retimonocolpites-type pollen from the early Cretaceous of Portugal: missing link in the eumagnoliid tree? Grana 50(1): 3-29.
Friis, E. M., K. R. Pedersen, and P. R. Crane. 2000. Fossil floral structures of a basal angiosperm with monocolpate, reticulate-acolumellate pollen from the early Cretaceous of Portugal. Grana 39: 226-245.
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.
Horikx, M., P. A. Hochuli, S. Feist-Burkhardt, and U. Heimhofer. 2016. Albian angiosperm pollen from shallow marine strata in the Lusitanian Basin, Portugal. Review of Palaeobotany and Palynology 228: 67–92.
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.
Kvaček, J., J. A. Doyle, P. K. Endress, V. Daviero-Gomez, B. Gomez, and M. Tekleva. 2016. Pseudoasterophyllites cretaceus from the Cenomanian of the Czech Republic: a possible link between Chloranthaceae and Ceratophyllum. Taxon 65(6): 1345-1373.
Kvaček, J. and E. M. Friis. 2010. Zlatkocarpus gen. nov., a new angiosperm reproductive structure with monocolpate-reticulate pollen from the late Cretaceous (Cenomanian) of the Czech Republic. Grana 49(2): 115-127.
Lora, J., M. Herrero, and J. I. Hormaza. 2009. The coexistence of bicellular and tricellular pollen in Annona cherimola (Annonaceae): implications for pollen evolution. American Journal of Botany 96(4): 802-808.
Lu, L., A. H. Wortley, D-Z. Li, H. Wang, and S. Blackmore. 2015. Evolution of angiosperm pollen. 2. The basal angiosperms. Annals Missouri Botanical Garden 100(3): 227-269.
Marshall, C. R. 2008. A simple method for bracketing absolute divergence times on molecular phylogenies using multiple fossil calibration points. American Naturalist 171: 726-742.
Marshall, C. R. 2010. Using confidence intervals to quantify the uncertainty in the end-points of stratigraphic ranges. Pp. 291-316 In: J. Alroy and G. Hunt (eds.), Quantitative Methods in Paleobiology, The Paleontological Society Papers, Volume 16. New Haven: The Paleontological Society, 316 pp.
Massoni, J., J. A. Doyle, and H. Sauquet. 2015. Fossil calibration of Magnoliidae, an ancient lineage of angiosperms. Palaeontologica Electronica 18.1.2FC.
Miller, J. M. 1989. The archaic flowering plant family Degeneriaceae: its bearing on an old enigma. National Geographic Research 5(2): 218-231.
Müller, S., K. Salomo, J. Salazar, J. Naumann, M. A. Jaramillo, C. Neinhuis, T. S. Feild, and S. Wanke. 2015. Intercontinental long-distance dispersal of Canellaceae from the New to the Old World revealed by a nuclear single copy gene and chloroplast loci. Molecular Phylogenetics and Evolution 84: 205–219.
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.
Poole, I. and J. Francis. 2000. The first record of fossil wood of Winteraceae from the upper Cretaceous of Antarctica. Annals of Botany 85: 307-315.
Quental, T. B. and C. R. Marshall. 2010. Diversity dynamics: molecular phylogenies need the fossil record. Trends in Ecology and Evolution 25(8): 434-441.
Tekleva, M. V. and V. A. Krassilov. 2009. Comparative pollen morphology and ultrastructure of modern and fossil gnetophytes. Review of Palaeobotany and Palynology 156(1-2): 130-138.
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.
Walker, J. W., G. J. Brenner, and A. G. Walker. 1983. Winteraceous pollen in the Lower Cretaceous of Israel: early evidence of a magnolialean angiosperm family. Science 220: 1273-1275.
Wang, Yun, G. Fan, Y. Liu, F. Sun, C. Shi, X. Liu, J. Peng, W. Chen, X. Huang, S. Cheng, Y. Liu, X. Liang, H. Zhu, C. Bian, L. Zhong, T. Lv, H. Dong, W. Liu, X. Zhong, J. Chen, Z. Qan, Z. Wang, B. Tan, C. Lin, F. Mu, X. Xu, Y. Ding, A-Y. Guo, J. Wang, and W. Ke. 2013. The sacred lotus genome provides insight into the evolution of flowering plants. The Plant Journal 76: 557-567.
Wortley, A. H., H. Wang, L. Lu, D-Z. Li, and S. Blackmore. 2015. Evolution of angiosperm pollen. 1. Introduction. Annals Missouri Botanical Garden 100(3): 177-226.
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.
Zavada, M. S. and J. M. Benson. 1987. First fossil evidence for the primitive angiosperm family Lactoridaceae. American Journal of Botany 74(10): 1590-1594.
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.
To the left is a floral pair of Salvia uliginosa (Lamiaceae, Lamiales, Asteranae) in cultivation at the Butchart Gardens on Vancouver Island of western North America.
Inflorescences of fernleaf yarrows, Achillea filipendula (Asteraceae, Asterales, Asteranae), are pictured to the right. Cultivated at the Butchart Gardens on Vancouver Island of western North America, fernleaf yarrows were photographed in 1979 with a Nikkormat 35mm camera using Kodak ASA 25 film.
Except for reticulations, which are absent in the architecture of asterid capitulae, patterns of branching in compound inflorescences of fernleaf yarrows could be analogous to patterns of some paraphyletic clades of flowering plants.