Entomological Review

, Volume 96, Issue 4, pp 419–431 | Cite as

Features of the structure of hymenoptera associated with miniaturization: 2. Anatomy of Trichogramma evanescens (Hymenoptera, Trichogrammatidae)

  • A. A. PolilovEmail author


Anatomy of adults of Trichogramma evanescens (Hymenoptera: Trichogrammatidae) is described in detail for the first time based on series of sections and 3D computer reconstruction. The complex structure of the exoskeleton and musculature (except for reductions of individual muscles) is preserved in T. evanescens despite its tiny size. Considerable simplification is observed in the structure of the intestine, tracheal and circulatory systems, and in the reduced number of Malpighian tubules. Thus, the smallest Hymenoptera (Mymaridae and Trichogrammatidae) demonstrate both the effects of miniaturization universal for insects (reduction of the head endoskeleton, circulatory and respiratory systems) and specific ones.


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  1. 1.
    Beutel, R.G. and Vilhelmsen, L., “Head Anatomy of Xyelidae (Hexapoda: Hymenoptera) and Phylogenetic Implications,” Organisms Diversity and Evolution 7 3, 207–230 (2007).CrossRefGoogle Scholar
  2. 2.
    Boivin, G., “Reproduction and Immature Development of Egg Parasitoids,” Progress in Biological Control 9, 1–23 (2010).Google Scholar
  3. 3.
    Bradley, J.C., “The Wing Venation of Chalcidoidea and Some Allied Hymenoptera,” Mémoires de la Société Royale d’Entomologie de Belgique 27, 127–137 (1955).Google Scholar
  4. 4.
    Bucher, G., “The Anatomy of Monodontomerus dentipes Boh., an Entomophagous Chalcid,” Canadian Journal of Research 26, 230–281 (1948).CrossRefGoogle Scholar
  5. 5.
    Chumakova, B.M., “Comparative Anatomy and Biology of Trichogramma evanescens,” Trudy VIZR, No. 31, 164–182 (1968).Google Scholar
  6. 6.
    Flanders, S.E., “Notes on the Life History and Anatomy of the Trichogramma,” Annals of the Entomological Society of America 30 2, 304–308 (1937).CrossRefGoogle Scholar
  7. 7.
    Gibson, G.A.P., “Some Pro- and Mesothoracic Structures Important for Phylogenetic Analysis of Hymenoptera, with a Review of Terms Used for the Structures,” The Canadian Entomologist 117, 1395–1443 (1985).CrossRefGoogle Scholar
  8. 8.
    Gibson, G.A.P., “Evidence for Monophyly and Relationships of Chalcidoidea, Mymaridae, and Mymarommatidae (Hymenoptera: Terebrantes),” The Canadian Entomologist 118, 205–240 (1986).CrossRefGoogle Scholar
  9. 9.
    Gibson, G.A.P., “Sister-Group Relationship of the Platigastroidea and Chalcidoidea (Hymenoptera) — an Alternate Hypothesis to Rasnitsyn (1988),” Zoologica Scripta 28, 125–138 (1999).CrossRefGoogle Scholar
  10. 10.
    Gibson, G.A.P., Heraty, J.M., and Woolley, J.B., “Phylogenetics and Classification of Chalcidoidea and Mymarommatoidea — a Review of Current Concepts (Hymenoptera, Apocrita),” Zoologica Scripta 28 (1–2), 87–124 (1999).CrossRefGoogle Scholar
  11. 11.
    Gorodkov, K.B., “Oligomerization and Evolution of Morphological Systems. 2. Oligomerization and Decrease in Body Size,” Zoologicheskii Zhurnal 63 12, 1765–1778 (1984).Google Scholar
  12. 12.
    Hanna, A.D., “The Male and Female Genitalia and the Biology of Euchalcidia caryobori Hanna (Hymenoptera, Chalcidinae),” Transactions of the Royal Entomological Society of London 82, 107–136 (1934).CrossRefGoogle Scholar
  13. 13.
    Hanna, A.D., “The Morphology and Anatomy of Euchalcidia caryobori Hanna (Hymenoptera- Chalcidinae),” Bulletin de la Societe Royale Entomologique d’Egypte 19, 326–361 (1935).Google Scholar
  14. 14.
    Heraty, J.M., Burks, R.A., Cruaud, A., Gibson, G.A.P., Liljeblad, J., et al., “A Phylogenetic Analysis of the Megadiverse Chalcidoidea (Hymenoptera),” Cladistics 29, 1–77 (2013).CrossRefGoogle Scholar
  15. 15.
    Heraty, J.M., Ronquist, F., Carpenter, J.M., Hawks, D., Schulmeister, S., et al., “Evolution of the Hymenopteran Megaradiation,” Molecular Phylogenetics and Evolution 60, 73–88 (2011).CrossRefPubMedGoogle Scholar
  16. 16.
    Ivanova-Kazas, O.M., “Postembryonic Development of Prestwichia aquatica Lubb. (Hymenoptera),” Trudy Leningradskogo Obshchestva Estestvoispytatelei 71 4, 165–213 (1952).Google Scholar
  17. 17.
    James, H.C., “The Anatomy of a British Phytophagous Chalcidoid of the Genus Harmolita (Isosoma),” Proceedings of the Zoological Society of London 96 1, 75–182 (1926).CrossRefGoogle Scholar
  18. 18.
    Lino-Neto, J., Bao, S.N., and Dolder, H., “Structure and Ultrastructure of the Spermatozoa of Trichogramma pretiosum and Trichogramma atopovirilla (Hymenoptera: Trichogrammatidae),” Acta Zoologica 81, 205–211 (2000).CrossRefGoogle Scholar
  19. 19.
    Lino-Neto, J. and Dolder, H., “Redescription of Sperm Structure and Ultrastructure of Trichogramma dendrolimi (Hymenoptera: Chalcidoidea: Trichogrammatidae),” Acta Zoologica 82, 159–164 (2001).CrossRefGoogle Scholar
  20. 20.
    Makarova, A.A. and Polilov, A.A., “Peculiarities of the Brain Organization and Fine Structure in Small Insects Related to Miniaturization. 2. The Smallest Hymenoptera (Mymaridae, Trichogrammatidae),” Zoologicheskii Zhurnal 92 6, 695–706 (2013) [Entomological Review 93 6, 714–724 (2013)].Google Scholar
  21. 21.
    Munro, J.B., Heraty, J.M., Burks, R.A., Hawks, D., Mottern, J., Cruaud, A., Rasplus, J.-Y., and Jansta, P., “A Molecular Phylogeny of the Chalcidoidea (Hymenoptera),” PLoS ONE 6 (11), e27023 (2011).CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Nagarkatti, S. and Nagaraja, H., “Biosystematics of Trichogramma and Trichogrammatoidea Species,” Annual Review of Entomology 22 1, 157–176 (1977).CrossRefGoogle Scholar
  23. 23.
    Nikolskaya, M.N., Chalcid Wasps of the Fauna of the USSR (Chalcidoidea) (USSR Academy of Sciences, Moscow, 1952) [in Russian].Google Scholar
  24. 24.
    Noyes, J.S. and Valentine, E.W., “Chalcidoidea (Insecta: Hymenoptera): Introduction, and Review of Genera in Smaller Families,” Fauna of New Zealand 18, 1–91 (1989).Google Scholar
  25. 25.
    Pinto, J.D., “A Review of the New World Genera of Trichogrammatidae (Hymenoptera),” Journal of Hymenoptera Research 15, 38–163 (2006).Google Scholar
  26. 26.
    Polilov, A.A., “Anatomy of the Feather-Winged Beetles Acrotrichis montandoni and Ptilium myrmecophilum (Coleoptera, Ptiliidae),” Zoologicheskii Zhurnal 84 2, 181–189 (2005) [Entomological Review 85 5, 467–475 (2005)].Google Scholar
  27. 27.
    Polilov, A.A., “Morphological Specificity of Mymaridae Related to Miniaturization,” in Studies of Hymenoptera: Collected Works (KMK Scientific Press, Moscow, 2007), pp. 50–64 [in Russian].Google Scholar
  28. 28.
    Polilov, A.A., “Anatomy of the Smallest Coleoptera, Featherwing Beetles of the Tribe Nanosellini (Coleoptera, Ptiliidae), and Limits of Insect Miniaturization,” Zoologicheskii Zhurnal 87 2, 181–188 (2008) [Entomological Review 88 1, 26–33 (2008)].Google Scholar
  29. 29.
    Polilov, A.A., “The Smallest Insects Evolve Anucleate Neurons,” Arthropod Structure and Development 41, 27–32 (2012).Google Scholar
  30. 30.
    Polilov, A.A., “Morphological Features of Insects Associated with Miniaturization,” Vestnik Moskovskogo Universiteta, Seriya 16. Biologiya, No. 3, 37–43 (2015a).Google Scholar
  31. 31.
    Polilov, A.A., “Small is Beautiful: Features of the Smallest Insects and Limits to Miniaturization,” Annual Review of Entomology 60, 103–121 (2015b).CrossRefPubMedGoogle Scholar
  32. 32.
    Polilov, A.A., “Features of the Structure of Hymenoptera Associated with Miniaturization. 1. Anatomy of the Fairyfly Anaphes flavipes (Hymenoptera, Mymaridae),” Zoologicheskii Zhurnal 95 5, 567–578 (2016) [Entomological Review 96 4, 407–418 (2016)].Google Scholar
  33. 33.
    Polilov, A.A. and Beutel, R.G., “Miniaturization Effects in Larvae and Adults of Mikado sp. (Coleoptera: Ptiliidae), One of the Smallest Free-Living Insects,” Arthropod Structure and Development 38, 247–270 (2009).CrossRefPubMedGoogle Scholar
  34. 34.
    Polilov, A.A. and Beutel, R.G., “Developmental Stages of the Hooded Beetle Sericoderus lateralis (Coleoptera: Corylophidae) with Comments on the Phylogenetic Position and Effects of Miniaturization,” Arthropod Structure and Development 39, 52–69 (2010).CrossRefPubMedGoogle Scholar
  35. 35.
    Rasnitsyn, A.P., “The Origin and Evolution of the Hymenoptera,” Trudy Paleontologicheskogo Instituta Akademii Nauk SSSR 174, 1–192 (1980).Google Scholar
  36. 36.
    Rasnitsyn, A.P. and Brothers, D.J., “Two New Hymenopteran Fossils from the Mid-Cretaceous of Southern Africa (Hymenoptera: Jurapriidae, Evaniidae),” African Invertebrates 48 1, 193–202 (2007).Google Scholar
  37. 37.
    Rasnitsyn, A.P., Basibuyuk, H.H., and Quicke, D.L.J., “A Basal Chalcidoid (Insecta: Hymenoptera) from the Earliest Cretaceous or Latest Jurassic of Mongolia,” Insect Systematics and Evolution 35, 123–135 (2004).CrossRefGoogle Scholar
  38. 38.
    Ronquist, F., Klopfstein, S., Vilhelmsen, L., Schulmeister, S., Murray, D.L., and Rasnitsyn, A.P., “A Total- Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera,” Systematic Biology 61 6, 973–999 (2012).CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Sharkey, M.J., Carpenter, J.M., Vilhelmsen, L., Heraty, J., Liljeblad, J., et al., “Phylogenetic Relationships among Superfamilies of Hymenoptera,” Cladistics 28 1, 80–112 (2012).CrossRefGoogle Scholar
  40. 40.
    Sorokina, A.P., A Key to Species of the Genus Trichogramma Westw. (Hymenoptera, Trichogramma) of the World Fauna (Kolos, Moscow, 1993) [in Russian].Google Scholar
  41. 41.
    Vilhelmsen, L., Miko, I., and Krogmann, L., “Beyond the Wasp-Waist: Structural Diversity and Phylogenetic Significance of the Mesosoma in Apocritan Wasps (Insecta: Hymenoptera),” Zoological Journal of the Linnean Society 159 1, 22–194 (2010).CrossRefGoogle Scholar

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© Pleiades Publishing, Inc. 2016

Authors and Affiliations

  1. 1.Faculty of BiologyLomonosov Moscow State UniversityMoscowRussia

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