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Phylogeny of Higher Taxa in Insecta: Finding Synapomorphies in the Extant Fauna and Separating Them from Homoplasies

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Abstract

Most currently applied systematic methods use post-groundplan character states to reconstruct phylogenies in modern higher Insecta/Arthropoda taxa. But, this approach is unable to separate synapomorphies from frequently occurring homoplasies. Conflicting, unresolved and unrealistic higher-level phylogenies result. The reasons are analyzed. A contrasting “groundplan” method, long used in Vertebrata and found to be superior in resolving higher-level phylogenies, is described. This method, as used for insects, uses a highly diversified morphological organ system (such as limb/wing), identifies its homologues in all subphyla and classes, records the full history of its character transformation series in all lineages from the shared Paleozoic ancestor to modern times, pursues the full homologization of its character states in all modern orders, and verifies these data with evidence from other fields of biology. Only such an extremely broad dataset provides the complex information needed to identify and homologize the groundplan character states in modern orders and other higher taxa in the insect/arthropod fauna. After this is accomplished, the gate to recognizing higher-level synapomorphies is open. Only groundplan-level character states include distinct synapomorphies, since homoplasies are either absent or easily detectable. Examples are given. The interpretations of higher phylogenies and evolutionary processes in Hexapoda, based on the unpredictable and often misleading post-groundplan character states found in extant, Tertiary and Mesozoic fauna, are critically compared with those based on the evolution of organ systems, by using the groundplan method.

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References

  • Abouheif, E., & Wray, G. A. (2002). Evolution of the gene network underlying wing polyphenism in ants. Science, 297, 249–252.

    Article  PubMed  CAS  Google Scholar 

  • Averov, M., & Cohen, M. (1997). Evolutionary origin of wings from ancestral gills. Nature, 385, 627–630.

    Article  Google Scholar 

  • Bechly, G., Brauckmann, C., Zessin, W., & Gröning, E. (2001). New results concerning the morphology of the most ancient dragonflies (Insecta: Odonatoptera from the Namurian of Hagen-Vorhalle (Germany). Journal of Zoology, Systematic Evolutionary Research, 39, 209–226.

    Article  Google Scholar 

  • Benton, M. (2003). When life nearly died. London: Thames & Hudsoon, 330 p.

  • Beutel, R. G., & Pohl, H. (2006). Endopterygote systematics—Where do we stand and what is the goal (Hexapoda, Arthropoda)? Systematic Entomology, 31, 202–219.

    Article  Google Scholar 

  • Bininda-Emonds, O. R. P., Bryant, H. N., & Russel, A. P. (1998). Supraspecific taxa as terminals in cladistic analysis: implicit assumptions of monophyly and a comparison method. Biological Journal of the Linnean Society, 64, 101–133.

    Google Scholar 

  • Bocharova-Messner, O. M. (1959). Development of the wing in the early postembryonic stage in the ontogeny of dragonflies (order Odonata). Institut Morfologii Zhitelnych Imeni Severtsova, 27, 187–200, in Russian.

    Google Scholar 

  • Boudreaux, H. B. (1979). Arthropod phylogeny with special references to Insects. New York: Wiley & Sons, 320 p.

  • Brodsky, A. K. (1994). The evolution of insect flight. Oxford: Oxford University Press, 229 p.

  • Carpenter, F. M. (1992). Treatise of invertebrate paleontology, superclass Hexapoda, part R, Arthropoda, 3. Boulder, Colorado: The Geological Society of America, 655 p.

  • Carpenter, F. M., & Richardson, E. S. (1968). Megasecopterous nymphs in Pennsylvanian concretions from Illinois. Psyche, 75, 295–309.

    Google Scholar 

  • Carpenter, F. M., & Richardson, E. S. (1971). Additional insects in Pennsylvanian concretions from Illinois. Psyche, 78, 267–295.

    Google Scholar 

  • CSIRO. (1991). The insects of Australia. The textbook for students and research workers. Naumann, I. F. (Chief Ed.). Melbourne University Press, Melbourne, 1137 p.

  • Erwin, D. H. (1993). The Great Paleozoic Crisis. Life and death in the Permian. Columbia University Press, 327 p.

  • Garcia-Beillido, A. (1975). Genetic control of wing disc development in Drosophila. In Cell Patterning. Ciba Foundation Symposium, Vol. 29, pp. 161–182.

  • Grimaldi, D., & Engel, M. S. (2005). Evolution of the insects. New York: Cambridge University Press, 755 p.

  • Haas, F., & Kukalová-Peck, J. (2001). Dermaptera hindwing structure and folding: new evidence for familial, ordinal and superordinal relationships within Neoptera (Insecta). European Journal of Entomology, 98, 445–509.

    Google Scholar 

  • Hennig, W. (1969). Die Stammesgeschichte der Insekten. Frankfurt am Main: Kramer, 436 p.

  • Hennig, W. (1981). Insect phylogeny. New York: Wiley & Sons, 514 p.

  • Hovmöler, R., Pape, T., & Kallersjö, M. (2002). The Paleoptera problem: basal pterygote phylogeny inferred from 18S and 28S rDNA sequences. Cladistics, 18, 313–323.

    Google Scholar 

  • Kjer, K. M. (2004). Aligned 18S and insect phylogeny. Systematic Biology, 53(3), 506–514.

    Article  PubMed  Google Scholar 

  • Kingsolver, J. G., & Koehl, M. A. R. (1994). Selective factors in the evolution of insect wings. Annual Review of Entomology, 39, 425–451.

    Article  Google Scholar 

  • Kristensen, N. P. (1991). Phylogeny of extant hexapods. The insects of Australia. A textbook for students and research workers (2nd ed.), Vol. 1. Melbourne: Melbourne University Press, pp. 125–140.

  • Kristensen, N. P. (1995). Forty years’ insect phylogenetic systematics. Zoologische Beitrage, (N.F.), 36, 83–124.

    Google Scholar 

  • Kristensen, N. P. (1998). The groundplan and basal diversification of the hexapods. In R. A. Fortey, & R. H. Thomas (Eds.), Arthropod Relationships (pp. 281–293). London: Chapman & Hall.

    Google Scholar 

  • Kukalová-Peck, J. (1969). Revisional study of the order Palaeodictyoptera in the Upper Carboniferous shales of Commentry, France. Part I. Psyche, 76(2), 163–215.

    Article  Google Scholar 

  • Kukalová-Peck, J. (1970). Revisional study of the order Palaeodictyoptera in the Upper Carboniferous shales of Commentry, France. Part II and III. Psyche, 76, 439–486; 77, 1–44.

    Google Scholar 

  • Kukalová-Peck, J. (1974). The order Megasecoptera (Insecta) from the Lower Permian of Moravia with description of new families and nymphal development. Psyche, 82, 1–19.

    Google Scholar 

  • Kukalová-Peck, J. (1978). Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record. Journal of Morphology, 156, 53–126.

    Article  Google Scholar 

  • Kukalová-Peck, J. (1983). Origin of the insect wing and wing articulation from the arthropodan leg. Canadian Journal of Zoology, 62, 618–1669.

    Google Scholar 

  • Kukalová-Peck, J. (1985). Ephemeroid wing venation based upon new gigantic Carboniferous mayflies and basic morphology, phylogeny, and metamorphosis of pterygote insects (Insecta, Ephemerida). Canadian Journal of Zoology, 63, 993–955.

    Google Scholar 

  • Kukalová-Peck, J. (1987). New Carboniferous Diplura, Monura, and Thysanura, the hexapod ground plan, and the role of thoracic lobes in the origin of wings (Insecta). Canadian Journal of Zoology, 65, 2327–2345.

    Google Scholar 

  • Kukalová-Peck, J. (1991). Fossil history and the evolution of hexapod structures. The Insects of Australia. A textbook for students and research workers (2nd ed.), Vol. l. Melbourne: Melbourne University Press, pp. 41–179.

  • Kukalová-Peck, J. (1992). The “Uniramia” do not exist: the groundplan of Pterygota as revealed by the Permian Diaphanopterodea from Russia (Insecta: Paleodictyopteroidea). Canadian Journal of Zoology, 70, 236–255.

    Google Scholar 

  • Kukalová-Peck, J. (1998). Arthropod phylogeny and “basal” morphological structures. Arthropod Relationships. In R. A. Fortey & R. H Thomas (Eds.), London: Chapman & Hall pp. 249–268.

  • Kukalová-Peck, J., & Brauckmann, C. (1990). Wing folding in pterygote insects, and the oldest Diaphanopterodea from the early Late Carboniferous of West Germany. Canadian Journal of Zoology, 68, 1104–1111.

    Article  Google Scholar 

  • Kukalová-Peck, J., & Brauckmann, C. (1992). Most Paleozoic Protorthoptera are ancestral hemipteroids: Major wing braces as clues to a new phylogeny of Neoptera (Insecta). Canadian Journal of Zoology, 70, 2452–2473.

    Google Scholar 

  • Kukalová-Peck, J., & Lawrence, J. F. (2004). Relationship among coleopteran suborders and major endoneopteran lineages: Evidence from hind wing characters. European Journal of. Entomology, 101, 95–144.

    Google Scholar 

  • Kukalová-Peck, J., & Richardson, E. S. Jr. (1983). New Homoiopteridae (Insecta: Paleodictyoptera) with wing articulation from Upper Carboniferous strata of Mazon Creek, Illinois. Canadian Journal of Zoology, 61, 670–687.

    Google Scholar 

  • Maas, A., Waloszek, D., & Müller, K. J. (2003). Morphology, ontogeny and phylogeny of the Phosphatocopina (Crustacea) from Upper Cambrian ‘Orten’ of Sweden. Fossils and Strata, 49, 1–238.

    Google Scholar 

  • Manton, S. M. (1977). The Arthropoda. Habits, functional morphology and evolution. Oxford: Clarendon Press, 527 p.

  • Marden, J. H. (1995). Flying lessons from a flightless insect. Natural History, 2(95), 6–8.

    Google Scholar 

  • Marden, J. H. (2003). The surface-skimming hypothesis for the evolution of insect flight. Acta zoologica cracoviensia, 46(Suppl.-Fossil Insects), 73–84.

    Google Scholar 

  • Marshall, C. R., Raff, E. C., & Raff, R. A. (1994). Dollo’s law and the death and resurrection of genes. Proceedings of National Academy of Sciences, USA, 91, 1283–1287.

    Article  Google Scholar 

  • Martynov, A. V. (1923). On two basic types of insect wings and their significance for the general classification of insects. In: Deryugina, K. M. (Ed.), Trudy Pervogo Vserossijskogo S’ezda Zoologov, Anatomov i Gistologov, Vol. 1, pp. 88–89.

  • Martynov, A. V. (1924). Über zwei Grundtypen der Flügel bei den Insekten und ihre Evolution. Zeitschrift für Morphologie und Oekologie, 4, 465–501.

    Article  Google Scholar 

  • Martynov, A. V. (1931). New Permian Paleoptera with the discussion of some problems of their evolution. Trudy Paleozoologicheskogo Instituta, 1, 1–44.

    Google Scholar 

  • Norling, U. (1982). Structure and ontogeny of the lateral abdominal gills and the caudal gill in Euphaeidae (Odonata: Zygoptera) larvae. Zoologisches Jahrbuch Anatomy, 107, 343–389.

    Google Scholar 

  • Paganiban, G. A., Serbin, L., Nagy, I., & Caroll, S. (1995). The evolution and patterning of insect limbs. Current Biology, 4, 671–675.

    Article  Google Scholar 

  • Popadić, A. G., Paganiban, G. A. Rush, Shear, W. A., & Kaufmann, T. C. (1998). Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Development Genes and Evolution, 208, 42–150.

    Google Scholar 

  • Prendini, L. (2001). Species or supraspecific taxa as terminals in cladistic analysis? Groundplans versus exemplars revisited. Systematic Biology, 50, 290–300.

    Article  PubMed  CAS  Google Scholar 

  • Raff, R. A. (1996). The shape of life. Genes, development, and the evolution of animal form. University of Chicago Press, 520 p.

  • Raff, R. A., Wray, G. A., & Henry, J. J. (1991). Implications of radical evolutionary changes in early development for concepts of developmental constraints. In L. Waren & H. Koprowski (Eds.), New perspectives on evolution (pp. 189–207). New York: Wiley-Liss.

    Google Scholar 

  • Riek, E. F., & Kukalová-Peck, J. (1984). A new interpretation of dragonfly wing venation based upon Early Upper Carboniferous fossils from Argentina (Insecta: Odonatoidea) and basic character states in pterygote wings. Canadian Journal of Zoology, 62, 1150–1166.

    Article  Google Scholar 

  • Ross, H. H. (1974). Biological systematics. Addison-Wesley Publishing Company, Inc., 345 pp.

  • Schwartz, J. H., & Maresca, B. (2006). Do molecular clocks run at all? A critique of molecular systematics. Biological Theory, 1(4), 357–371.

    Article  Google Scholar 

  • Sharov, A. G. (1957). Peculiar Paleozoic wingless insects of the new order Monura (Insecta, Apterygota. Doklady Akademii Nauk USSR, 115, 796–798.

    Google Scholar 

  • Sharov, A. G. (1966). Basic arthropodan stock. London: Pergamon Press, 271 p.

  • Shear, W. A., & Kukalová-Peck, J. (1990). The ecology of Paleozoic terrestrial arthropods: The fossil evidence. Canadial Journal of Zoology, 68, 1807–1934.

    Google Scholar 

  • Shubin, N. H., Tabin, C., & Carroll, S. B. (1997). Fossils, genes and the evolution of animal limbs. Nature, 388, 639–648.

    Article  PubMed  CAS  Google Scholar 

  • Smith, E. L. (1970). Biology and structure of some California bristletails and silverfish. Pan-Pacific Entomologist, 46, 212–225.

    Google Scholar 

  • Smith, E. L. (1988). Morphology and evolution of the hexapod head. In: Proceedings of the 18th International Congress on Entomology, Vancouver, 73 p.

  • Snodgrass, R. E. (1935). Principles of insect morphology. New York: Mc Graw-Hill, 667 p.

  • Stenzhorn, H. J. (1974). Experimentelle Untersuchungen zur Entwicklung des Lymantria dispar L. (Lepidoptera). Wilhelm Roux Archive, Entwicklungen Mechanische Organisation, 175, 65–86.

    Article  Google Scholar 

  • Šulc, K. (1927). Das Tracheensystem von Lepisma (Thysanura) und Phylogenie der Pterygogenea. Acta Societatis Scientifica Naturalis Moravicae, 4(7/39), 108 p.

  • Tower, W. L. (1903). The origin and development of the wings in Coleoptera. Zoologisches Jahrbuch, Anatomy, 17, 517–572.

    Google Scholar 

  • Wägele, J. W. (1993). Rejection of the “Uniramia” hypothesis and implications of the Mandibulata concept. Zoologisches Jahrbuch, Systematik, 120, 253–288.

    Google Scholar 

  • Wägele, J. W. (1996). First principles of phylogenetic systematics, a basis of numerical methods used for morphological and molecular characters. Vie Milieu, 46(2), 125–138.

    Google Scholar 

  • Webster, M. (2007). A Cambrian peak in morphological variation within trilobite species. Science, 317, 499–502.

    Article  PubMed  CAS  Google Scholar 

  • Wheeler, Q. D. (2004). Taxonomic triage and the poverty of phylogeny. Philosophical Transactions of the Royal Society of London, B, 359, 571–583.

    Article  Google Scholar 

  • Wheeler, W. C., Whiting, M., Wheeler, Q. D., & Carpenter, J. M. (2000). The phylogeny of the extant hexapod orders. Cladistics, 17, 13–169.

    Google Scholar 

  • Williams, J. A., & Carroll, S. B. (1993). The origin, patterning and evolution of insect appendages. Biological Essays, 15, 567–577.

    Google Scholar 

  • Willmann, R. (1997). Advances and problems in insect phylogeny. Arthropod relationships. In: R. A. Fortey & R. H. Thomas (Eds.) London: Chapman & Hall, pp. 69–279.

  • Wootton, R. J., & Kukalová-Peck, J. (2000). Flight adaptations in Palaeozoic Palaeoptera (Insecta). Biological Reviews, 75, 129–167.

    Article  PubMed  CAS  Google Scholar 

  • Wootton, R. J., Kukalová-Peck, J., Newman, D. J. S., & Muzon, P. (1998). Smart engineering in the Mid-Carboniferous: how well could Palaeozoic dragonflies fly? Science, 282, 749–751.

    Article  PubMed  CAS  Google Scholar 

  • Yeates, D. K. (1995). Groundplans and exemplars: path of the tree of life. Cladistics, 11, 343–357.

    Article  Google Scholar 

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Acknowledgements

Broad evolutionary-morphological contributions in insects are quite impossible without selfless and massive help from systematists specializing in individual orders. I am deeply obliged to many entomologists who, over the years, by their suggestions and their wonderful insect collections, have helped to clarify for me the theoretical and practical aspects of the groundplan method. This includes my past and present co-authors and friends, who patiently shared with me their extensive knowledge of modern and fossil entomofaunas. This essay would never be possible without the profound morphological analysis of arthropods by Edward Laidlaw Smith (The California Academy of Sciences, San Francisco), which I had the privilege to witness and participate in, and without my field assistant Karel Havlata, who organized the fossil excavations in Moravia. Because of my politically challenged origins, my international background in Paleozoic insects was possible only with the most generous support of Frank M. Carpenter, Harvard University, Cambridge, and Ernst Mayr, Museum of Comparative Zoology, Cambridge. With their grant I also studied, over multiple prolonged visits, all Paleozoic insects deposited at the Muséum d’Histoire Naturelle, Paris, at the Palentological Institute, Moscow (with B. B. Rohdendorf and A. G. Sharov), and at the Museum of Natural History, London. My work in Canada was supported by the Canadian NSERC grant agency, and by Stewart B. Peck, Carleton University, Ottawa. The grants made it possible for me to study extensively Paleozoic insects in Russia, Germany, on many occasions at the Field Museum, Chicago (with E. S. Richardson) and in numerous private collections in the Chicago area. Fossils and rare primitive hemipteroids were researched at The Australian Museum, Sydney (Australia), and at the Natal Museum, Pietermaritzburg (South Africa). Modern insects were collected extensively in North, Central, and South America, including Alaska, Yukon, Tierra del Fuego, Galápagos Islands, Puerto Rico, Dominican Republic, Jamaica, Cuba, Lesser Antilles, South Africa and Ghana, all around Australia, New Zealand, New Caledonia, Fiji, Lord Howe Island, Japan, and China. I studied extensively in several months-long visits, modern Ephemeroptera at the Florida A&M University, Tallahassee (with J. & J. Peters) and at the Czech Academy of Sciences, České Budějovice (Czech Republic) (with T. Soldán), modern Coleoptera (with J. F. Lawrence), orthopteroids (with D. Rentz) at CSIRO, Canberra, and orthopteroids, blattoids and Dermaptera at the Academy of Sciences, Philadelphia (with D. Otte and F. Haas). Orthopteroids and tropical Hemipteroids were studied in Prague (with P. Štys), at INBIO, Santo Domingo, Costa Rica, and at the Territorial Museum, Darwin, peloridiids in Sydney (Australia) (with J. Evans), DSIR Auckland (New Zealand) (with W. Kuschel), and in the Bishop Museum, Honolulu (with S. Miller). At the Smithonian Institution, Washington, D.C., I studied Mecoptera and Trichoptera (with O. Flint), orthopteroids (with D. Nickles), and Carboniferous insects (with C. Labandeira). Plecoptera were researched at the Max Planck Institute, Schlitz, Germany (with P. Zwick), Embioptera at the California Academy of Sciences, San Francisco (with E.S. Ross), and Neuroptera and Megaloptera mainly in Ottawa (on material delivered by K. Lambkin). Hymenoptera were researched in the collection of Agriculture, Canada, Ottawa (with M. Sharkey and G. Gibson). My friend Jan G. Peters, Florida A&M University, Tallahassee devoted many hours to reviewing this manuscript. G. S. Ball and B. S. Heming, University of Alberta, Edmonton, R.G. Beutel, Friedrich Schiller Universität, Jena, and V.A. Grebenikov, Agriculture and Agri-Food Canada, Ottawa provided critical remarks and important pointers in contemporary systematic methods. From G. Bechly, Museum für Naturkunde, Stuttgart, I received useful suggestions clarifying some terms. I also received invaluable editorial help from B. Hallgrimsson, and from two reviewers who devoted generously their time to improve the presentation of arguments. To all these colleagues, co-authors and friends, and others too many to be named, goes my sincere gratitude and thanks.

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Kukalová-Peck, J. Phylogeny of Higher Taxa in Insecta: Finding Synapomorphies in the Extant Fauna and Separating Them from Homoplasies. Evol Biol 35, 4–51 (2008). https://doi.org/10.1007/s11692-007-9013-4

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