[ Publication of the Year ]
Each year I will select a scientific paper, book chapter, or book as being of paramount importance toward solving enigmatic origins of angiosperms and understanding the paleobiology of interacting holometabolous insects including phytophagy, pollenivory, and coevolution of arthropod/seed plant molecular tool kits and body plans. My annual selection is stated and discussed in the section that follows this floristic, geologic, and paleobiogeographic note.
Spectacular outcrops of the 40 million year old Sespe Formation are composed of purplish conglomerate rock exposures. Rounded cobbles, lenticular gravels, and water-worn pebbles and sands of the conglomerate, probably owe their shapes to scouring from the Colorado Paleoriver.
Sandstone cliffs have kept the incidence of catastrophic wildfire to a minimum allowing three pinids to survive on ledges and crevices of rock formations in this area. 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 Topa Topa Mountains. North America's Transverse Ranges including this detached block of the Sespe Formation, support populations of Santa Ynez false lupine. Populations of Thermopsis macrophylla (Fabaceae, Fabales, Rosanae) indigenous to the Sespe's rugged Bear Heaven are of interest to students of biogeography, botany, ecology, and systematics.
The Outstanding Scientific Paper of 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).
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?
"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).
These reading selections may be of interest:
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.
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.
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.
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.
The scanning electron micrograph shown above is the anterior front part of the head of Haptoncus tahktajanii (Nitidulidae, Coleoptera), the cucujiform phytophagous associate of the primitive magnoliid flowering plant Degeneria vitiensis (Degeneriaceae, Magnoliales, Magnoliidae). Some of the gustatory, olfactory, and visual sensory organs of the nitidulid beetle are visible including antennae, sensillae, compound eyes, mandibles, maxillae, and labia.
Previous Publication of the Year:
Four significant conclusions from a study of molecular phylogenies of the WOX family of homeodomain proteins 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.
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 image was captured by the author in 1970 using Kodak ASA 25 film as part of a biome project conducted by Allen Cattel, Richard May, John 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.
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