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The origins of insect metamorphosis

Abstract

Insect metamorphosis is a fascinating and highly successful biological adaptation, but there is much uncertainty as to how it evolved. Ancestral insect species did not undergo metamorphosis and there are still some existing species that lack metamorphosis or undergo only partial metamorphosis. Based on endocrine studies and morphological comparisons of the development of insect species with and without metamorphosis, a novel hypothesis for the evolution of metamorphosis is proposed. Changes in the endocrinology of development are central to this hypothesis. The three stages of the ancestral insect species—pronymph, nymph and adult—are proposed to be equivalent to the larva, pupa and adult stages of insects with complete metamorphosis. This proposal has general implications for insect developmental biology.

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Figure 1: Comparison of the early immature stages of ametabolous, hemimetabolous and holometabolous insect species.
Figure 2: Endocrinology of embryonic and post-embryonic insect development.
Figure 3: The effects of the JH mimic pyriproxifen on Locusta embryos.
Figure 4: Relationship of the phylogeny of the Holometabola to the pattern of imaginal disc formation.
Figure 5: Possible steps in the transition from a hemimetabolous to a holometabolous life history and their relationship to timing of JH production (blue bar) and to growth directed towards the imaginal form (black triangles).

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References

  1. Carpenter,F. M. in Treatise on Invertebrate Paleontology. Part R, Arthropoda 4 Vol. 3 Superclass Hexapoda 1–277 (Geological Soc. Am., Boulder, Colorado, 1992).

    Google Scholar 

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

    Article  Google Scholar 

  3. Kristensen,N. P. The phylogeny of hexapod “orders”. A critical review of recent accounts. Z. Zool. Systematic Evolutionsforschung 13 , 1–44 (1975).

    Google Scholar 

  4. Berlese,A. Intorno alle metamorfosi degli insetti. Redia 9, 121–136 (1913).

    Google Scholar 

  5. Poyarkoff,E. Essai d'une théorie de la nymphe des Insectes Holométaboles. Arch. Zool. Exp. Gen. 54, 221–265 (1914).

    Google Scholar 

  6. Hinton,H. E. On the origin and function of the pupal stage. Trans. R. Entomol. Soc. Lond. 99, 395–409 ( 1948).

    Article  Google Scholar 

  7. Hinton,H. E. Biology of Insect Eggs Vol. 1 (Pergamon, Oxford, 1981).

    Google Scholar 

  8. Hinton,H. E. On the structure, function, and distribution of the prolegs of the Panorpoidea with a criticism of the Berlese–Imms theory. Trans. R. Entomol. Soc. Lond. 106, 455–545 (1955).

    Article  Google Scholar 

  9. Sehnal,F. in Comprehensive Insect Physiology, Biochemistry, and Pharmacology Vol. 2 (eds Kerkut, G. A. & Gilbert, L. I.) 1– 86 (Pergamon, Oxford, 1985).

    Google Scholar 

  10. Sehnal,F., Svácha,P. & Zrzavy,J. in Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells (eds Gilbert, L. I., Tata, J. R. & Atkinson, B. G.) 3–58 (Academic, San Diego, 1996).

    Book  Google Scholar 

  11. Novak,V. J. A. Insect Hormones 2nd English edn (Chapman and Hall, London, 1975).

    Google Scholar 

  12. van der Hammen,L. An Introduction to Comparative Arachnology (SPB, The Hague, 1989).

    Google Scholar 

  13. Heeley,W. Observations of the life-histories of some terrestrial isopods. Proc. Zool. Soc. Lond. 111, 79–149 (1941).

    Google Scholar 

  14. Lindsay,E. The biology of the silverfish, Ctenolepisma longicaudata Esch. with particular reference to its feeding habits. Proc. R. Soc. Victoria 52, 35–83 ( 1940).

    Google Scholar 

  15. Bernays,E. A. The vermiform larva of Schistocerca gregaria (Forskål): Form and activity (Insecta, Orthoptera). Z. Morph. Tiere. 70, 183–200 (1971).

    ADS  Google Scholar 

  16. Sbrenna,G. in Morphogenetic Hormones of Arthropods Vol. 3 (ed. Gupta, A. P.) 44–80 (Rutgers Univ. Press, New Brunswick, New Jersey, 1991).

    Google Scholar 

  17. Sbrenna-Micciarelli,A. & Sbrenna,G. The embryonic apolyses of Schistocerca gregaria (Orthoptera). J. Insect Physiol. 18, 1027–1037 ( 1972).

    Article  Google Scholar 

  18. Edwards,J. S. & Chen, S.-W. Embryonic development of an insect sensory system, the abdominal cerci of Acheta domesticus. Wilhelm Roux Arch. Dev. Biol. 186, 151–178 (1979).

    Article  Google Scholar 

  19. Dorn,A. & Hoffmann,P. The ‘embryonic moults’ of the milkweed bug as seen by the S.E.M. Tiss. Cell 13, 461–473 (1981).

    Article  CAS  Google Scholar 

  20. Heming,B. S. Structure and development of larval antennae in embryos of Lytta viridana LeConte (Coleoptera: Meloidae). Can. J. Zool. 74, 1008–1034 (1996).

    Article  Google Scholar 

  21. Campos-Ortega,J. A. & Hartenstein,V. The Embryonic Development of Drosophila melanogaster (Springer, Berlin, 1985).

    Book  Google Scholar 

  22. Broadie,K. S., Bate,M. & Tublitz,N. J. Quantitative staging of embryonic development of the tobacco hawkmoth, Manduca sexta. Wilhelm Roux Arch. Dev. Biol. 199, 327–334 (1991).

    Article  Google Scholar 

  23. Meier,T., Chabaud,F. & Reichert, H. Homologous patterns in the embryonic development of the peripheral nervous system in the grasshopper Schistocerca gregaria and the fly Drosophila melanogaster. Development 112, 241–253 (1991).

    CAS  PubMed  Google Scholar 

  24. Bate,C. M. Pioneer neurones in an insect embryo. Nature 260, 54–56 (1976).

    Article  ADS  CAS  Google Scholar 

  25. Grueber,W. B. & Truman,J. W. Identification and development of a nitric oxide-sensitive peripheral plexus in larvae of the moth, Manduca sexta. J. Comp. Neurol. 404, 127– 141 (1999).

    Article  CAS  Google Scholar 

  26. Kutsch,W. & Bentley,D. Programmed death of peripheral pioneer neurons in the grasshopper embryo. Dev. Biol. 123, 517–525 (1987).

    Article  CAS  Google Scholar 

  27. Zacharuk,R. Y. & Shields,V. D. Sensilla of immature insects. Annu. Rev. Entomol. 36, 331–354 (1991).

    Article  Google Scholar 

  28. Nijhout,H. F. Insect Hormones (Princeton Univ. Press, Princeton, New Jersey, 1994).

    Google Scholar 

  29. Riddiford,L. M. Cellular and molecular actions of juvenile hormone. I. General considerations and premetamorphic actions. Adv. Insect Physiol. 24 , 213–274 (1994).

    Article  CAS  Google Scholar 

  30. Lagueux,M., Hetru,H., Goltzené,F., Kappler,C. & Hoffmann, J. A. Ecdysone titre and metabolism in relation to cuticulogenesis in embryos of Locusta migratoria. J. Insect Physiol. 25, 709–725 (1979).

    Article  CAS  Google Scholar 

  31. Temin,G., Zander,M. & Roussel,J. P. Physico-chemical (GC-MS) measurements of juvenile hormone III titres during embryogenesis of Locusta migratoria. Int. J. Invert. Reprod. 9, 105–112 (1986).

    Article  CAS  Google Scholar 

  32. Imboden,H., Lanzrein,B., Delbecque,J. P. & Lüscher,M. Ecdysteroids and juvenile hormone during embryogenesis in the ovoviviparous cockroach Nauphoeta cinerea. Gen. Comp. Endocrinol. 36, 628–635 (1978).

    Article  CAS  Google Scholar 

  33. Dorn,A. Hormones during embryogenesis of the milkweed bug, Oncopeltus fasciatus (Heteroptera: Lygaeidae). Entomol. Gen. 8, 193– 214 (1983).

    Google Scholar 

  34. Novák,V. J. A. Morphological analysis of the effects of juvenile hormone analogues and other morphologically active substances on embryos of Schistocerca gregaria Forsk. J. Embryol. Exp. Morphol. 21, 1– 21 (1969).

    PubMed  Google Scholar 

  35. Sbrenna-Micciarelli,A. Effects of farnesyl methyl ether on embryos of Schistocerca gregaria (Orthoptera). Acta Embryol. Morphol. Exp. 3, 295–303 (1977).

    Google Scholar 

  36. Brüning,E., Saxer,A. & Lanzrein,B. Methyl farnesoate and juvenile hormone III in normal and precocene-treated embryos of the ovoviviparous cockroach Nauphoeta cinerea . Int. J. Invert. Reprod. Dev. 8, 269 –278 (1985).

    Article  Google Scholar 

  37. Bergot,B. J., Baker,F. C., Cerf,D. C., Jamieson,G. & Schooley, D. A. in Juvenile Hormone Biochemistry (eds Pratt, G. E. & Brooks, G. T.) 33–45 (Elsevier, Amsterdam, 1981).

    Google Scholar 

  38. Riddiford,L. M. in Insect Juvenile Hormones, Chemistry and Action (eds Menn, J. J. & Beroza, M.) 95–111 (Academic, New York, 1972).

    Book  Google Scholar 

  39. Riddiford,L. M. & Williams,C. M. The effects of juvenile hormone on the embryonic development of silkworms. Proc. Natl Acad. Sci. USA 57, 595– 601 (1967).

    Article  ADS  CAS  Google Scholar 

  40. Smith,R. F. & Arking,R. The effects of juvenile hormone analogues on the embryogenesis of Drosophila melanogaster. J. Insect Physiol. 21, 723–732 ( 1975).

    Article  CAS  Google Scholar 

  41. Oberlander,H. in Comprehensive Insect Physiology, Biochemistry, and Pharmacology Vol. 2 (eds Kerkut, G. A. & Gilbert, L. I.) 151– 182 (Pergamon, Oxford, 1985).

    Google Scholar 

  42. Kurushima,M. & Ohtaki,T. Relation between cell number and pupal development of wing disks in Bombyx mori. J. Insect Physiol. 21, 1705–1712 ( 1975).

    Article  Google Scholar 

  43. Kremen,C. & Nijhout,H. F. Control of pupal commitment in the imaginal disks of Precis coenia (Lepidoptera: Nymphalidae). J. Insect Physiol. 44, 287–298.

  44. Svácha,P. What are and what are not imaginal discs: reevaluation of some basic concepts (Insecta, Holometabola). Dev. Biol. 154, 101–117 (1992).

    Article  Google Scholar 

  45. Quennedey,A. & Quennedey,B. Morphogenesis of the wing anlagen in the mealworm beetle Tenebrio molitor during the last larval instar. Tiss. Cell 22, 721–740 (1990).

    Article  CAS  Google Scholar 

  46. Monsma,S. A. & Booker,R. Genesis of the adult retina and outer optic lobes of the moth, Manduca sexta. I. Patterns of proliferation and cell death. J. Comp. Neurol. 367, 10 –20 (1996).

    Article  CAS  Google Scholar 

  47. Champlin,D. T. & Truman,J. W. Ecdysteroids govern two phases of eye development during metamorphosis of the moth, Manduca sexta. Development 125, 2009 –2018 (1998).

    CAS  PubMed  Google Scholar 

  48. Reddy,G., McCaleb,D. C. & Kumaran, A. K. Tissue distribution of juvenile hormone hydrolytic activity in Galleria mellonella larvae. Experientia 36, 461–462 (1980).

    Article  CAS  Google Scholar 

  49. Tower,W. L. The origin and development of the wings of Coleoptera. Zool. Jahrb. 17, 515–572 ( 1903).

    Google Scholar 

  50. Carroll,S. B. Homeotic genes and the evolution of arthropods and chordates. Nature 376, 479–485 ( 1995).

    Article  ADS  CAS  Google Scholar 

  51. Couso,J. P. & Bishop,S. A. Proximal–distal development in the legs of Drosophila. Int. J. Dev. Biol. 42, 345–352 (1998).

    CAS  PubMed  Google Scholar 

  52. Rohdendorf,E. B. & Sehnal,F. Inhibition of reproduction and embryogenesis in the firebrat, Thermobia domestica. J. Insect Physiol. 19, 37–56 (1973).

    Article  CAS  Google Scholar 

  53. Watson,J. A. L. The growth and activity of the corpora allata in the larval firebrat, Thermobia domestica (Packard) (Thysanura, Lepismatidae). Biol. Bull. 132, 277–291 ( 1967).

    Article  CAS  Google Scholar 

  54. Durston,A. J., van der Wees,J., Pijnappel, W. W. M. & Godsave,S. F. Retinoids and related signals in early development of the vertebrate central nervous system. Curr. Top. Dev. Biol. 40, 111–175 (1998).

    Article  CAS  Google Scholar 

  55. Needham,J. G., Traver,J. R. & Hsu, Y.-C. The Biology of Mayflies (Comstock, Ithaca, New York, 1935).

    Google Scholar 

  56. Asahina,S. A Morphological Study of a Relic Dragonfly Epiophlebia superstes Selys (Odonata, Anisozygoptera) (Japan Soc. Promotion Sci., Tokyo, 1954).

    Google Scholar 

  57. Vaught,G. L. & Stewart,K. W. The life history and ecology of the stonefly, Neoperla clymene (Newman) (Plecoptera: Perlidae). Ann. Entomol. Soc. Am. 67, 167–178 (1974).

    Article  Google Scholar 

  58. Corbert,P. S. The immature stages of the emperor dragonfly, Anax imperator Leach (Odonata: Aeshnidae). Entomol. Gazet. 6, 189–197 (1955).

    Google Scholar 

  59. Azam,K. M. & Anderson,N. H. Life history and habits of Sialis rotunda and S. californica in Western Oregon. Ann. Entomol. Soc. Am. 62, 549–558 (1969).

    Article  Google Scholar 

  60. Riddiford,L. M. & Truman,J. W. in Insect Biochemistry (ed. Rockstein, M.) 307–357 (Academic, New York, 1978).

    Book  Google Scholar 

  61. Bollenbacher,W. E., Smith,S. L., Goodman,W. & Gilbert,L. I. Ecdysteroid titer during the larval–pupal–adult development of the tobacco hornworm, Manduca sexta. Gen. Comp. Endocrinol. 44, 302–306 (1981).

    Article  CAS  Google Scholar 

  62. Baker,F. C., Tsai,L. W., Reuter,C. C. & Schooley,D. A. In vivo fluctuation of JH, JH acid, and ecdysteroid titer, and JH esterase activity during development of fifth stadium Manduca sexta. Insect Biochem. 17, 989–996 ( 1987).

    Article  CAS  Google Scholar 

  63. Fain,M. J. & Riddiford,L. M. Juvenile hormone titers in the hemolymph during later larval development of the tobacco hornworm, Manduca sexta (L.). Biol. Bull. 149, 506– 521 (1975).

    Article  CAS  Google Scholar 

  64. Whiting,M. F., Carpenter,J. C., Wheeler, Q. D. & Wheeler,W. C. The strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst. Biol. 46, 1–68 ( 1997).

    CAS  PubMed  Google Scholar 

  65. Lawrence,J. F. & Newton,A. F. Evolution and classification of beetles. Annu. Rev. Ecol. Syst. 13 , 261–290 (1982).

    Article  Google Scholar 

  66. Powell,P. B. The development of the wings of certain beetles, and some studies of the origin of the wings of insects. J. N.Y. Entomol. Soc. 12, 237–243; 13, 5–22 (1904, 1905).

    Google Scholar 

  67. Tiegs,O. W. Researches on the insect metamorphosis. I. On the structure and post-embryonic development of a chalcid wasp, Nasonia. Trans. R. Soc. South Australia 46, 319–527 ( 1922).

    Google Scholar 

  68. Dewitz,H. Beiträge zur postembryonalen Gliedmassenbildung bei den Insecten. Z. Wiss. Zool. 30, 78–105 (1878).

    Google Scholar 

  69. Karawaiew,W. Die nachembryonale Entwicklung von Lasius flavus. Z. Wiss. Zool. 64, 385–478 ( 1898).

    Google Scholar 

  70. Meyer,D. R., Sachs,F. N. & Rohner, R. M. Parameters for growth of the imaginal wing disk in last instar larvae of Galleria mellonella L. J. Exp. Zool. 213, 185–197 ( 1980).

    Article  CAS  Google Scholar 

  71. Williams,C. M. in Insect Biology in the Future (eds Locke, M. & Smith, D. S.) 369–384 (Academic, New York, 1980).

    Book  Google Scholar 

  72. Mercer,W. F. The development of the wings in the Lepidoptera. New York Entomol. Soc. 8, 1–20 ( 1900).

    Google Scholar 

  73. Weismann,A. Die metamorphose von Corethra plumicornis. Z. Wiss. Zool. 16, 1–83 (1866 ).

    Google Scholar 

  74. Neumann,D. & Spindler, K.-D. Circasemilunar control of imaginal disc development in Clunio marinus: Temporal switching point, temperature-compensated developmental time and ecdysteroid profile. J. Insect Physiol. 37, 101–109 ( 1991).

    Article  CAS  Google Scholar 

  75. Bryant,P. J. Cell lineage relationships in the imaginal wing disc of Drosophila melanogaster . Dev. Biol. 22, 389– 411 (1970).

    Article  CAS  Google Scholar 

  76. Weismann,A. Die nachembryonale Entwicklung der Musciden nach Beobachtungen an Musca vomitoria und Sarcophaga carnaria. Z. Wiss. Zool. 14, 101–263 (1864).

    Google Scholar 

  77. Pratt,H. S. Imaginal discs in insects. Psyche 8, 15– 30 (1897).

    Article  Google Scholar 

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Acknowledgements

We thank E. Ball for use of facilities at the Australian National University during the experimental phase of this study and for extensive comments on the manuscript. We also thank J. Edwards, J. Kingsolver, L. Nagy and D. Erezyilmaz for comments on drafts of this paper. This article is dedicated to the late G. B. Craig Jr, an inspirational force in the research and teaching of entomology.

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Truman, J., Riddiford, L. The origins of insect metamorphosis. Nature 401, 447–452 (1999). https://doi.org/10.1038/46737

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