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The evolutionary role and fate of the primary ovipositor in insects

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Abstract

The development of a piercing-sawing ovipositor for introducing eggs into living plant tissues has made its owners independent of the soil characteristics and increased egg protection. This was the most important prerequisite for the appearance of wings and flight which provided the winged insects with tremendous opportunities for finding new niches and led to unparalleled adaptive radiation. The ovipositor has passed several stages of improvement and differentiation. The four principal types of the primary ovipositor are considered: those of Odonata, Diaphanopteroidea (only extinct forms), Cicadina (including Paraneoptera and Hymenoptera), and Orthoptera. A new hypothesis of the gonangulum homologies is put forward, interpreting it as half of sternite IX lateral of the midline plus the paratergite of the same segment. The constructions of the valvae and different homologies of the third valvae in Polyneoptera and Eumetabola are discussed. The primary ovipositor has been repeatedly (i.e., in many lineages) reduced in the evolution of Pterygota. The main circumstances of these reductions are: (1) subterranean (fossorial) life in narrow cavities; (2) aquatic life of the larvae, mostly linked with submerged oviposition; (3) development and perfection of flight to which the heavy and protruding ovipositor was a hindrance. All the holometabolous insects except Hymenoptera lack the primary ovipositor.

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References

  1. An Encyclopedic Dictionary of Biology (Sovetskaya Entsiklopediya, Moscow, 1986), p. 93 [in Russian].

  2. Ander, K., “Vergleichen-anatomische und phylogenetische Studien über die Ensifera (Saltatoria),” Opusc. Entomol. Suppl. 2, 1–306 (1939).

    Google Scholar 

  3. Anisyutkin, L.N. and Gorochov, A.V., “On the Supposed Evolutionary Scenario of the Origin of Higher Taxa within Dictyoptera,” in Modern Paleontology: The Classical and Latest Methods. The First All-Russian School, 2004 (Moscow, 2005), pp. 109–116 [in Russian].

    Google Scholar 

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

    Google Scholar 

  5. Austin, A.D. and Browning, T.O., “A Mechanism for Movement of Eggs along Insect Ovipositors,” Int. J. Insect Morphol. Embryol. 10(2), 93–108 (1981).

    Google Scholar 

  6. Badonnel, A., “Ordre de Psocoptères,” in Traité de zoologie, anatomie, systématique, biologie, Ed. by P. Grassé, Vol. 10 (1951), pp. 1301–1340.

    Google Scholar 

  7. Badonnel, A., “Psocoptera,” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen (Munksgaard, Copenhagen, 1956), pp. 143–145.

    Google Scholar 

  8. Badonnel, A., “Psocoptera,” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen, 2nd ed. (Munksgaard, Copenhagen, 1970), pp. 172–175.

    Google Scholar 

  9. Bechly, C., Brauckmann, C., Zessin, W., and Groning, E., “New Results Concerning the Morphology of the Most Ancient Dragonflies (Insecta: Odonatoptera) from the Namurian of Hagen-Vorhalle (Germany),” J. Zool. Syst. Evol. Res. 39, 209–226 (2001).

    Google Scholar 

  10. Becker, E.G., “On the Structure and Origin of External Genital Appendages of Thysanura and Hymenoptera,” Trudy Nauchno-Issled. Inst. Zool. Mos. Gos. Univ. 1, 157–206 (1925).

    Google Scholar 

  11. Becker-Migdisova, E.E., “The Phylogeny of Psyllomorpha as Related to Their Trophic Adaptation to Host Plants,” in A Conference Dedicated to the Centenary of Academician A.A. Borisyak (Moscow, 1972), pp. 3–4.

    Google Scholar 

  12. Bedford, G.O., “Biology and Ecology of the Phasmatodea,” Annu. Rev. Entomol. 23, 135–149 (1978).

    Google Scholar 

  13. Bey-Bienko, G.Ya., Insecta: Dictyoptera (Fauna of the USSR, New Series, Vol. 40) (Moscow, 1950) [in Russian].

    Google Scholar 

  14. Bitsch, C. and Bitsch, J., “The Phylogenetic Interrelationships of the Higher Taxa of Apterygote Hexapods,” Zool. Scripta 29(2), 131–156 (2000).

    Google Scholar 

  15. Bitsch, J., “Morphologie abdominale de machilides (Insecta Thysanura) — I. Squelette et musculature des segments pregenitaux,” Ann. Sci. Nat. 12, 173–200 (1973).

    Google Scholar 

  16. Bitsch, J., “Morphologie abdominalle des machilides (Thysanura) — II. Squelette et musculature des segments genitaux femelles,” Int. J. Insect Morph. Embryol. 3, 101–120 (1974).

    Google Scholar 

  17. Brauckmann, C., “Morphologie und Variabilität von Homoioptera vorhallensis (Insecta: Palaeodictyoptera: Ober Karbon),” Geol. Palaeontol. 25, 193–215 (1991).

    Google Scholar 

  18. Cappe de Baillon, P., “Contribution anatomique et physiologique à l’étude de la reproduction chez les Locustiens et les Grylloniens. I,” Cellule 31(1), 1–245 (1920).

    Google Scholar 

  19. Cappe de Baillon, P., “Contribution anatomique et physiologique à l’étude de la reproduction chez les Locustiens et les Grylloniens. II,” Cellule 32(1), 1–193 (1922).

    Google Scholar 

  20. China, W.E., “South American Peloridiidae (Hemiptera-Homoptera: Coleorrhyncha),” Trans. R. Entomol. Soc. London 114(5), 131–161 (1962).

    Google Scholar 

  21. Chopard, L., “La biologie des Orthopteres,” Encycl. Entomol. Ser. A 20, 1–541 (1938).

    Google Scholar 

  22. Delany, M.J., “The Life Histories and Ecology of Two Species of Petrobius Leach, P. brevistylis and P. maritimus,” Trans. R. Soc. Edinburgh 63(3), 501–533 (1960).

    Google Scholar 

  23. Deuve, Th., “Sur la présence d’un ‘épipleurite’ dans le plan de base du segment des Hexapodes,” Bull. Entomol. Soc. France 99(2), 199–210 (1994).

    Google Scholar 

  24. Deuve, Th., “The Epipleural Field in Hexapods,” Ann. Entomol. Soc. France N. S. 37(1–2), 195–231 (2001).

    Google Scholar 

  25. Dupuis, Cl., “Heteroptera,” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen, 2nd ed. (Munksgaard, Copenhagen, 1970), pp. 190–209.

    Google Scholar 

  26. Emeljanov, A.F., “The Phylogeny of Cicadina (Homoptera) Based on Comparative Morphological Data,” Trudy Vses. Entomol. Obshch. 69, 19–109 (1987).

    Google Scholar 

  27. Emeljanov, A.F., “Some Macroevolutionary Modes Related to Repeated and Novel Use of Once Acquired Structures,” in Third Meeting in Memory of A.A. Lyubischev (Togliatti, 2000), pp. 60–64 [in Russian].

    Google Scholar 

  28. Feuerstein, V., “Morphology of Female Terminalia of Nymphes myrmeleonoides Leach, 1814 (Neuroptera, Nymphidae) and Phylogenetic Implications,” Ann. Mus. Civ. Nat. Ferrara 8, 55–58 (2007).

    Google Scholar 

  29. Flower, J.W., “On the Origin of Flight in Insects,” J. Insect Physiol. 10, 81–88 (1964).

    Google Scholar 

  30. Fraser, F.C., “Odonata,” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen (Munksgaard, Copenhagen, 1956), pp. 32–37.

    Google Scholar 

  31. Gorb, S.N., “Egg Transporting Microstructures of the Odonate Ovipositor,” Petalura 2, 1–3 (1996).

    Google Scholar 

  32. Gorochov, A.V., “The Primitive Titanoptera and the Early Evolution of Polyneoptera,” in N.A. Kholodkovsky Memorial Lectures, Vol. 57, Issue 1 (2004), pp. 3–53 [in Russian].

    Google Scholar 

  33. Günther, K., “Cheleutoptera (Phasmoidea),” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen (Munksgaard, Copenhagen, 1956), pp. 49–52.

    Google Scholar 

  34. Historical Development of the Class Insecta, Ed. by B.B. Rohdendorf and A.P. Rasnitsyn (Nauka, Moscow, 1980) [in Russian].

    Google Scholar 

  35. History of Insects, Ed. by A.P. Rasnitsyn and D.L.J. Quicke (Kluwer Academic Publishers, Dordrecht etc., 2002).

    Google Scholar 

  36. Hünefeld, F., Missbach, Ch., and Beutel, G., “The Morphology and Evolution of the Female Postabdomen of Holometabola (Insecta),” Arthropod Structure Dev. 41, 361–371 (2012).

    Google Scholar 

  37. Hughes, L. and Westoby, M., “Capitula on Stick Insect Eggs and Elaiosomes on Seeds: Convergent Adaptations for Burial by Ants,” Function. Ecol. 6, 642–648 (1992).

    Google Scholar 

  38. Inward, D., Beccaloni, G., and Eggleton, P., “Death of an Order: a Comprehensive Molecular Phylogenetic Study Confirms that Termites are Eusocial Cockroaches,” Biol. Letters 3(3), 331–335 (2007).

    CAS  Google Scholar 

  39. Johnson, C., “Breeding Behavior and Oviposition in Hetaerina americana (Fabricius) and H. titia (Drury) (Odonata: Agriidae),” Canad. Entomol. 93, 260–266 (1961).

    Google Scholar 

  40. Kaplin, V.G., “On the Classification and Phylogeny of Bristletails of the Family Machilidae (Thysanura, Microcoryphia),” Entomol. Obozr. 64(2), 336–350 (1985).

    Google Scholar 

  41. Kaplin, V.G., “On the Fauna of the Bristletail Family Nicoletiidae (Thysanura) of Thailand,” Zool. Zh. 91(5), 544–553 (2012) [Entomol. Rev. 92 (9), 966–976 (2012)].

    Google Scholar 

  42. Klass, K.-D., “The Female Genitalic Region in Basal Earwigs (Insecta: Dermaptera: Pygidicraniidae s. l.),” Entomol. Abhandl. 61(2), 173–225 (2003).

    Google Scholar 

  43. Klass, K.-D., “The Female Abdomen of Ovipositor-Bearing Odonata (Insecta: Pterygota),” Arthropod Syst. Phyl. 66(1), 45–142 (2008).

    Google Scholar 

  44. Klass, K.-D. and Matushkina, N.A., “The Exoskeleton of the Female Genitalic Region in Petrobiellus takunagae (Insecta: Archaeognatha): Insect-Wide Terminology, Homologies, and Functional Interpretations,” Arthropod Structure Dev. 41, 575–591 (2012).

    Google Scholar 

  45. Klass, K.-D., Matushkina, N.A., and Raidel, J., “The Gonangulum: A Reassessment of Its Morphology, Homology, and Significance,” Arthropod Structure Dev. 41, 373–394 (2012).

    Google Scholar 

  46. Kluge, N.J., The Modern Taxonomy of Insects (Lan, St. Petersburg, 2000) [in Russian].

    Google Scholar 

  47. Koteja, J., “Essay on the Prehistory of the Scale Insects (Homoptera, Coccinea),” Ann. Zool. Warszawa 38(15), 461–503 (1985).

    Google Scholar 

  48. Kramer, S., “The Morphology and Phylogeny of Auchenorrhynchous Homoptera (Insecta),” Illinois Biol. Monographs 20(4), 1–111 (1950).

    Google Scholar 

  49. Kukalova-Peck, J. and Brauckmann, C., “Most Paleozoic Protorthoptera are Ancestral Hemipteroids: Major Wing Braces as Clues to a New Phylogeny of Neoptera (Insecta),” Canad. J. Zool. 68, 2452–2473 (1992).

    Google Scholar 

  50. LaGreca, M., “Origin and Evolution of Wings and Flight in Insects,” Boll. Zool. Suppl. 47, 65–82 (1980).

    Google Scholar 

  51. Matsuda, R., “Morphology and Evolution of the Insect Thorax,” Mem. Entomol. Soc. Canada, No. 76, 1–431 (1970).

    Google Scholar 

  52. Matsuda, R., Morphology and Evolution of the Insect Abdomen (Pergamon Press, 1976).

    Google Scholar 

  53. Matushkina, N.A., “Comparative Morphology of Ovipositors of Some Damselflies (Odonata, Zygoptera),” Vestnik Zool. 38(3), 53–66 (2004).

    Google Scholar 

  54. Matushkina, N.A., “Regular Egg-Positioning by an Aeshnid Species (Odonata, Aeshnidae) with Comments on Its Phylogenetic Value,” Vestnik Zool. 41(5), 457–462 (2007).

    Google Scholar 

  55. Matushkina, N.A., “The Ovipositor of the Relict Dragonfly Epiophlebia superstes: a Morphological Reexamination (Odonata, Epiophlebiidae),” Int. J. Odonatol. 11(1), 71–80 (2008a).

    Google Scholar 

  56. Matushkina, N.A., “Skeletomuscular Development of Genital Segments in the Dragonfly Anax imperator (Odonata, Aeshnidae) during Metamorphosis and Its Implications for the Evolutionary Morphology of the Insect Ovipositor,” Arthropod Structure Dev. 37, 321–332 (2008b).

    Google Scholar 

  57. Matushkina, N.A., “Ovipositor Internal Microsculpture in the Relic Silverfish Tricholepidion gertschi (Insecta: Zygentoma),” Psyche 2011, Article ID 563852 (2011), doi:10.1155/2011/563852.

    Google Scholar 

  58. Matushkina, N.A. and Gorb, S.N., “The Skeleto-Muscular Morphology of the Endophytic Ovipositor in Dragonflies (Odonata),” Vestnik Zool. 31(5–6), 57–70 (1997).

    Google Scholar 

  59. Matushkina, N.A. and Gorb, S.N., “A Classification of Endophytic Egg Layings of Damselflies (Odonata, Zygoptera),” Vestnik Zool. Suppl. 14, 152–159 (2000).

    Google Scholar 

  60. Matushkina, N.A. and Lambert, Ph.H., “Ovipositor Morphology and Egg Laying Behavior in the Dragonfly Lestes macrostigma (Zygoptera: Lestidae),” Int. J. Odonatol. 14(1), 69–82 (2011).

    Google Scholar 

  61. Meyen, S.V., Basic Paleobotany (Nedra, Moscow, 1987) [in Russian].

    Google Scholar 

  62. Michener, C.D., “Comparative External Morphology, Phylogeny and Classification of the Bees (Hymenoptera),” Bull. Amer. Mus. Nat. Hist. 82(6), 157–323 (1944).

    Google Scholar 

  63. Micoleit, G., “Über den Ovipositor der Neuropteroidea und Coleoptera und seine phylogenetische Bedeutung (Insecta, Holometabola),” Z. Morph. Tiere 74, 37–64 (1973a).

    Google Scholar 

  64. Micoleit, G., “Zur Anatomie und Funktion des Raphidiopteren-Ovipositors (Insecta, Neuropteroidea,” Z. Morph. Tiere 76, 145–171 (1973b).

    Google Scholar 

  65. Müller, H.J., “Über Bau und Funktion der Legeapparates der Zikaden (Homoptera, Cicadina),” Z. Ökol. Tiere 38(3), 534–629 (1942).

    Google Scholar 

  66. Nalepa, C.A. and Lenz, M., “The Ootheca of Mastotermes darwiniensis Froggatt (Isoptera: Mastotermitidae): Homology with Cockroach Oothecae,” Proc. Royal Soc. London 267, 1809–1813 (2000).

    CAS  Google Scholar 

  67. Pohl, L., “Vergleichende anatomisch-histologische Untersuchungen an Lepisma saccharina Linne und der mirmecophilen Atelura formicaria Heyden (Beitrag zur Mirmecophilie, erster Abschnitt),” Insect. Soc. 4, 349–363 (1957).

    Google Scholar 

  68. Ponomarenko, A.G., “Early Stages of Arthropod Evolution,” in Introduction to Paleoentomology, Ed. by V.V. Zherikhin, A.G. Ponomarenko, and A.P. Rasnitsyn (KMK Sci. Press, Moscow, 2008), pp. 254–278 [in Russian].

    Google Scholar 

  69. Popov, Yu.A., “Superorder Cimicidea,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980), pp. 58–69 [in Russian].

    Google Scholar 

  70. Priesner, H., “Thysanoptera,” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen (Munksgaard, Copenhagen, 1956), pp. 169–174.

    Google Scholar 

  71. Quicke, D.L.J., Fitton, M.G., Tunstead, J.R., et al., “Ovipositor Structure and Relationships within the Hymenoptera, with Special Reference to the Ichneumonidea,” J. Nat. Hist. 28, 635–682 (1994).

    Google Scholar 

  72. Rasnitsyn, A.P., “The Origin and Evolution of Lower Hymenopterans,” Trudy Paleontol. Inst. Akad. Nauk SSSR 123, 1–196 (1969).

    Google Scholar 

  73. Rasnitsyn, A.P., “Higher Hymenopterans of the Mesozoic,” Trudy Paleontol. Inst. Akad. Nauk SSSR 147, 1–132 (1975).

    Google Scholar 

  74. Rasnitsyn, A.P., “On the Early Evolution of Insects and the Origin of Pterygota,” Zh. Obshch. Biol. 37(4), 543–555 (1976).

    Google Scholar 

  75. Rasnitsyn, A.P., “The Origin and Evolution of Hymenoptera,” Trudy Paleontol. Inst. Akad. Nauk SSSR 174, 1–192 (1980a).

    Google Scholar 

  76. Rasnitsyn, A.P., “The Origin and Composition of the Class Insecta,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980b), pp. 19–20 [in Russian].

    Google Scholar 

  77. Rasnitsyn, A.P., “Class Scarabeoda Laicharting, 1781,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980c), pp. 20–21 [in Russian].

    Google Scholar 

  78. Rasnitsyn, A.P., “Subclass Scarabeona Laicharting, 1781,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980d), pp. 24–28 [in Russian].

    Google Scholar 

  79. Rasnitsyn, A.P., “Superorder Hypoperlidea Martynov, 1928,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980e), pp. 41–43 [in Russian].

    Google Scholar 

  80. Rasnitsyn, A.P., “Superorder Dictyoneuridea Handlirsch, 1906,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980f), pp. 43–44 [in Russian].

    Google Scholar 

  81. Rasnitsyn, A.P., “Superorder Vespidea Laicharting, 1781. Order Vespida Laicharting, 1781. The Hymenopterans,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980g), pp. 122–127 [in Russian].

    Google Scholar 

  82. Rasnitsyn, A.P., “Superorder Blattidea Latreille, 1810. Cockroaches,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980h), pp. 136–137 [in Russian].

    Google Scholar 

  83. Rasnitsyn, A.P., “Superorder Perlidea Latreille, 1802. Stoneflies,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980i), pp. 148–150 [in Russian].

    Google Scholar 

  84. Rasnitsyn, A.P., “Order Grylloblattida Walker, 1914,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980j), pp. 150–154 [in Russian].

    Google Scholar 

  85. Rasnitsyn, A.P. and Novokshonov, V.G., “On the Morphology of Uralia maculata (Insecta: Diaphanopterida) from the Early Permian (Kungurian) of Ural (Russia),” Entomol. Scand. 28, 27–38 (1997).

    Google Scholar 

  86. Rasnitsyn, A.P., “Class Insecta Linné, 1758. The Insects,” in History of Insects, Ed. by A.P. Rasnitsyn and D.L.J. Quicke (Kluwer Academic Publishers, Dordrecht etc., 2002), pp. 65–89.

    Google Scholar 

  87. Readio, P.A., “The Ovipositors of the Cicadellidae,” Bull. Kansas Univ. Sci. 14, 213–298 (1922).

    Google Scholar 

  88. Rehn, A., “Phylogenetic Analysis of the Higher-Level Relationships of Odonata,” Syst. Entomol. 28, 181–239 (2003).

    Google Scholar 

  89. Richards, O.W., “Hymenoptera, Introduction and Keys to Families,” in Handbooks for the Identification of British Insects. Vol. 6, Part 1 (1956), pp. 1–94.

    Google Scholar 

  90. Rousset, A., “Squelette et musculature de région génitales et postgénitales de la femelle de Thermobia domestica (Packard). Comparaison avec la région génitale de Nicoletia sp. (Insecta: Apterygota: Lepismatida),” Int. J. Insect Morphol. Embryol. 2(1), 55–80 (1973).

    Google Scholar 

  91. Scudder, G.G.E., “The Comparative Morphology of the Insect Ovipositor,” Trans. R. Entomol. Soc. London 113(2), 25–40 (1961a).

    Google Scholar 

  92. Scudder, G.G.E., “The Functional Morphology and Interpretation of the Insect Ovipositor,” Canad. Entomol. 93, 267–272 (1961b).

    Google Scholar 

  93. Scudder, G.G.E., “Grylloblattodea,” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen, 2nd ed. (Munksgaard, Copenhagen, 1970), pp. 55–58.

    Google Scholar 

  94. Sharov, A.G., Basic Arthropodan Stock with Special Reference to Insects (Pergamon Press, Oxford, 1966).

    Google Scholar 

  95. Sharov, A.G., “Phylogeny of Orthopteroid Insects,” Trudy Paleontol. Inst. Akad. Nauk SSSR 118, 1–217 (1968).

    Google Scholar 

  96. Shcherbakov, D.E. and Popov, Y.A., “Superorder Cimicidea Laicharting, 1781. Order Hemiptera Linne, 1758. The Bugs, Cicadas, Plantlice, Scale Insects etc.,” in History of Insects, Ed. by A.P. Rasnitsyn and D.L.J. Quicke (Kluwer Academic Publishers, Dordrecht etc., 2002), pp. 143–157.

    Google Scholar 

  97. Silvestri, F., “Thysanura,” Zool. Jahrb. 3(Suppl. 6), 773–786 (1905a).

    Google Scholar 

  98. Silvestri, F., “Materiali per lo studiodei Tisanuri. VI (1). Tre nuove specie di Nicoletia ad nuovo sottogenere,” Redia 2, 111–120 (1905b).

    Google Scholar 

  99. Silvestri, F., Compendio di entomologia applicata (agraria-forestale-medica-veterinaria) (Stab. Tip. Bellavista, Portici, 1934).

    Google Scholar 

  100. Sinichenkova, N.D., “Order Dictyoneurida Handlirsch, 1906,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980), pp. 44–47 [in Russian].

    Google Scholar 

  101. Smith, E.L., “Evolutionary Morphology of External Insect Genitalia. 1. Origin and Relationships to Other Appendages,” Ann. Entomol. Soc. Amer. 62, 1051–1079 (1969).

    Google Scholar 

  102. Snodgrass, R.E., Principles of Insect Morphology (Mc-Graw-Hill Book Comp. Inc., NY, 1935).

    Google Scholar 

  103. Spuris, Z.D., “Order Odonatoptera (Odonata): Dragonflies,” in Keys to Insects of the European Part of the USSR, in Five Volumes, Vol. 1, Ed. by G.Ya. Bey-Bienko (Nauka, Moscow, 1964), pp. 137–161 [in Russian].

    Google Scholar 

  104. Srivastava, V.K. and Srivastava, B.K., “External Genital Organs of Female Copera marginipes (Rambour) (Zygoptera: Platycnemididae),” Indian Odonatol. 2, 37–42 (1989).

    Google Scholar 

  105. Storozhenko, S.Yu., “Order Grylloblattida Walker, 1914,” in History of Insects, Ed. by A.P. Rasnitsyn and D.L.J. Quicke (Kluwer Academic Publishers, Dordrecht etc., 2002), pp. 278–281.

    Google Scholar 

  106. Sturm, H., and Bach de Roca, C., “On the Systematics of the Archaeognatha (Insecta),” Entomol. Gener. Stuttgart 18(1–2), 55–90 (1993).

    Google Scholar 

  107. Sturm, H. and Machida, R., “Archaeognatha,” in Handbuch der Zoologie, Vol. IV, Part 37 (Walter de Gruyter, Berlin, 2001), pp. 63–115.

    Google Scholar 

  108. St. Quentin, D., “Der Eilegeapparat der Odonaten,” Z. Morph. Ökol. Tiere 51, 165–189 (1962).

    Google Scholar 

  109. Štys, P., “Reinterpretation of the Theory of the Origin of the Pterygote Ovipositor and Notes on the Terminology of the Female Ectodermal Genitalia of Insects,” Acta Univ. Carol. Biol., No. 1, 75–85 (1959).

    Google Scholar 

  110. Szelegiewicz, H., “Cechy autapomorficzne w budowie skrzydeŁ Sternorrhyncha (Homoptera) i ich znaczenie dla oceny paleozoicznych przstawicieli tej grupy pluskwiaków,” Ann. Zool. Warszawa 29(2), 15–81 (1971).

    Google Scholar 

  111. Tillyard, R.J., The Biology of Dragonflies (Cambridge, 1917).

    Google Scholar 

  112. Tuxen, S.L., “Thysanura,” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen (Munksgaard, Copenhagen, 1956), pp. 21–23.

    Google Scholar 

  113. Vilhelmsen, L., “The Ovipositor Apparatus of Basal Hymenoptera (Insecta): Phylogenetic Implications and Functional Morphology,” Zool. Scripta 29, 319–345 (2000).

    Google Scholar 

  114. Vishnyakova, V.N., “New Species of the Genus Kunguroblattina from the Lower Permian of the Ural Region,” Paleontol. Zh. 4, 50–59 (1965).

    Google Scholar 

  115. Vishnyakova, V.N., “The Mesozoic Cockroaches (Blattodea) with an External Ovipositor and the Specific Traits of the Their Reproduction,” in The Jurassic Insects of Kara Tau, Ed. by B.B. Rohdendorf (Nauka, Moscow, 1968), pp. 55–86 [in Russian].

    Google Scholar 

  116. Vishnyakova, V.N., “Superorder Psocidea,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980a), pp. 52–57 [in Russian].

    Google Scholar 

  117. Vishnyakova, V.N., “Order Blattida,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980b), pp. 138–145 [in Russian].

    Google Scholar 

  118. Vishnyakova, V.N., “Order Psocoptera (Copeognatha),” in Keys to Insects of the Far East of the USSR, Vol. 1, Ed. by P.A. Lehr (Nauka, Moscow, 1986), pp. 323–357 [in Russian].

    Google Scholar 

  119. Walker, E.M., “The Terminal Abdominal Structures of Orthopteroid Insects: Phylogenetic Study, I,” Ann. Entomol. Soc. Amer. 12, 267–316 (1919).

    Google Scholar 

  120. Walker, E.M., “The Terminal Abdominal Structures of Orthopteroid Insects: Phylogenetic Study, II,” Ann. Entomol. Soc. Amer. 15, 1–76 (1922).

    Google Scholar 

  121. Walker, E.M., “Grylloblattaria,” in Taxonomist’s Glossary of Genitalia in Insects, Ed. by S.L. Tuxen (Munksgaard, Copenhagen, 1956), pp. 47–49.

    Google Scholar 

  122. Woicechowsky, W., “Studies on the Systematic System of Aphids (Homoptera, Aphidinea,” in Prace Naukowe Uniwersitetu Slaskiego w Ratowicach, No. 1269 (1992), pp. 3–75.

    Google Scholar 

  123. Wygodzinsky, P., “Beobachtungen an Spermatolophiden und Spermatophoren bei Nicoletiidae (Thysanura, Insecta),” Zool. Anz. 161, 280–287 (1958).

    Google Scholar 

  124. Wygodzinsky, P., “On a Surviving Representative of the Lepidotrichidae (Thysanura),” Ann. Entomol. Soc. Amer. 54(5), 621–627 (1961).

    Google Scholar 

  125. Zaitzev, A.A., http://flickrhivemind.net/user/A.Zaitsev, 2013.

  126. Zherikhin, V.V., “Insects in Terrestrial Ecosystems,” in Historical Development of the Class Insecta (Nauka, Moscow, 1980), pp. 189–224 [in Russian].

    Google Scholar 

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  1. Zoological Institute of the Russian Academy of Sciences, St. Petersburg, 199034, Russia

    A. F. Emeljanov

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Original Russian Text © A.F. Emeljanov, 2014, published in Zoologicheskii Zhurnal, 2014, Vol. 93, No. 1, pp. 91–130.

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Emeljanov, A.F. The evolutionary role and fate of the primary ovipositor in insects. Entmol. Rev. 94, 367–396 (2014). https://doi.org/10.1134/S0013873814030099

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