1932

Abstract

Miniaturization leads to considerable reorganization of structures in insects, affecting almost all organs and tissues. In the smallest insects, comparable in size to unicellular organisms, modifications arise not only at the level of organs, but also at the cellular level. Miniaturization is accompanied by allometric changes in many organ systems. The consequences of miniaturization displayed by different insect taxa include both common and unique changes. Because the smallest insects are among the smallest metazoans and have the most complex organization among organisms of the same size, their peculiar structural features and the factors that limit their miniaturization are of considerable theoretical interest to general biology.

Keyword(s): body sizeInsectamorphology
Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-010814-020924
2015-01-07
2024-06-22
Loading full text...

Full text loading...

/deliver/fulltext/ento/60/1/annurev-ento-010814-020924.html?itemId=/content/journals/10.1146/annurev-ento-010814-020924&mimeType=html&fmt=ahah

Literature Cited

  1. Bakkendorf O. 1.  1934. Biological investigations on some Danish hymenopterous egg-parasites, especially in homopterous and heteropterous eggs, with taxonomic remarks and descriptions of new species. Entomol. Medd. 19:1–134 [Google Scholar]
  2. Barber HS. 2.  1924. New Ptiliidae related to the smallest known beetle. Proc. Entomol. Soc. Wash. 26:6167–68 [Google Scholar]
  3. Bernstein S, Bernstein RA. 3.  1969. Relationships between foraging efficiency and the size of the head and component brain and sensory structures in the red wood ant. Brain Res. 16:185–104 [Google Scholar]
  4. Beutel RG, Haas A. 4.  1998. Larval head morphology of Hydroscapha natans LeConte 1874 (Coleoptera, Myxophaga, Hydroscaphidae) with special reference to miniaturization. Zoomorphology 118:2103–16 [Google Scholar]
  5. Beutel RG, Pohl H, Hunefeld F. 5.  2005. Strepsipteran brain and effect of miniaturization (Insecta). Arthropod Struct. Dev. 34:3301–13 [Google Scholar]
  6. Boivin G. 6.  2010. Reproduction and immature development of egg parasitoids. Egg Parasitoids in Agro-ecosystems with Emphasis on Trichogramma FL Consoli, JRP Parra, RA Zucchi 1–23 Prog. Biol. Control 9 Houten, Neth: Springer [Google Scholar]
  7. Borror DJ, DeLong DM, Triplehorn CA. 7.  1981. An Introduction to the Study of Insects Philadelphia: Saunders, 5th ed.. [Google Scholar]
  8. Bowestead S. 8.  1999. A Revision of the Corylophidae (Coleoptera) of the West Palaearctic Region Instrum. Biodivers. 3 Geneva: Mus. Hist. Nat. [Google Scholar]
  9. Burger JMS, Huang Y, Hemerik L, van Lenteren JC, Vet LEM. 9.  2006. Flexible use of patch-leaving decisions in a parasitoid wasp. J. Insect Behav. 19:155–70 [Google Scholar]
  10. Chetverikov SS. 10.  1920. The Fundamental Factor of Insect Evolution Washington, DC: Gov. Print. Off. [Google Scholar]
  11. Chittka L, Niven J. 11.  2009. Are bigger brains better?. Curr. Biol. 19:R995–1008 [Google Scholar]
  12. Chittka L, Skorupski P. 12.  2011. Information processing in miniature brains. Proc. R. Soc. B 278:885–88 [Google Scholar]
  13. Cole BJ. 13.  1986. Size and behavior in ants: constraints on complexity. Proc. Natl. Acad. Sci. USA 82:8548–51 [Google Scholar]
  14. Cuntz H, Forstner F, Schnell B, Ammer G, Raghu SV, Borst A. 14.  2013. Preserving neural function under extreme scaling. PLOS ONE 8:8e71540 [Google Scholar]
  15. De Marzo L. 15.  1992. Osservazioni anatomiche sui genitali interni maschili in alcuni Ptilidi (Coleoptera). Entomologica 27:107–15 [Google Scholar]
  16. Delvare G. 16.  1993. Guadeloupe avec la description d'une espèce nouvelle (Hymenoptera, Trichogrammatidae). Rev. Fr. Entomol. 15:149–52 [Google Scholar]
  17. Dogel' VA. 17.  1954. [Oligomerization of homologous organs as one of the main paths of evolution of animals] Leningrad: Leningrad Univ. Press
  18. Dozier HL. 18.  1932. Descriptions of new trichogrammatid (Hymenoptera) egg parasites from the West Indies. Proc. Entomol. Soc. Wash. 34:29–37 [Google Scholar]
  19. Dybas HS. 19.  1966. Evidence for parthenogenesis in the featherwing beetles, with a taxonomic review of a new genus and eight new species (Coleoptera: Ptiliidae). Fieldiana Zool. 51:11–52 [Google Scholar]
  20. Dybas LK, Dybas HS. 20.  1987. Ultrastructure of mature spermatozoa of a minute featherwing beetle from Sri Lanka (Coleoptera, Ptiliidae: Bambara). J. Morphol. 191:63–76 [Google Scholar]
  21. Eberhard WG. 21.  2007. Miniaturized orb-weaving spiders: behavioural precision is not limited by small size. Proc. R. Soc. B 274:2203–9 [Google Scholar]
  22. Eberhard WG. 22.  2011. Are smaller animals behaviourally limited? Lack of clear constraints in miniature spiders. Anim. Behav. 81:813–23 [Google Scholar]
  23. Eberhard WG, Wcislo WT. 23.  2011. Grade changes in brain–body allometry: morphological and behavioural correlates of brain size in miniature spiders, insects and other invertebrates. Adv. Insect Physiol. 40:155–214Reviews effects of body size on insect and spider nervous systems and spider behavior. [Google Scholar]
  24. Faisal AA, White JA, Laughlin SB. 24.  2005. Ion-channel noise places limits on the miniaturization of the brain's wiring. Curr. Biol. 15:121143–49 [Google Scholar]
  25. Fischer S, Meyer-Rochow VB, Müller CHG. 25.  2012. Challenging limits: ultrastructure and size-related functional constraints of the compound eye of Stigmella microtheriella (Lepidoptera: Nepticulidae). J. Morphol. 273:91064–78 [Google Scholar]
  26. Fischer S, Müller CHG, Meyer-Rochow VB. 26.  2011. How small can small be: the compound eye of the parasitoid wasp Trichogramma evanescens (Westwood, 1833) (Hymenoptera, Hexapoda), an insect of 0.3- to 0.4-mm total body size. Visual Neurosci. 28:4295–308 [Google Scholar]
  27. García-Barros E. 27.  2000. Body size, egg size, and their interspecific relationship with ecological and life history traits in butterflies (Lepidoptera: Papilionoidea, Hesperioidae). Biol. J. Linnean Soc. 70:251–84 [Google Scholar]
  28. García-Barros E. 28.  2002. Taxonomic patterns in the egg to body size allometry of butterflies and skippers (Papilionoidea & Hesperiidae). Nota Lepidopterol. 25:2/3161–75 [Google Scholar]
  29. Ghesquière J. 29.  1939. Contribution a l'étude des Hyménoptères du Congo Belge. VI. Déscription d'un Mymaride nouveau et remarques sur le Gn. Megaphragma Timb. (Trichogrammatidae). Rev. Zool. Bot. Afr. 35:33–41 [Google Scholar]
  30. Goossen H. 30.  1949. Untersuchungen an gehirnen verschieden grosser, jeweils verwandter Coleopteren- und Hymenopteren. Arten. Zool. Jb. Abt. Allg. Zool. 62:1–64 [Google Scholar]
  31. Gorodkov KB. 31.  1984. 2. [Oligomerization and evolution of the morphological structure systems. 2. Oligomerization and body size decrease]. Zool. Zhurnal 63:1765–78 [Google Scholar]
  32. Grebennikov VV. 32.  2008. How small you can go: factors limiting body miniaturization in winged insects with a review of the pantropical genus Discheramocephalus and description of six new species of the smallest beetles (Pterygota: Coleoptera: Ptiliidae). Eur. J. Entomol. 105:313–328 [Google Scholar]
  33. Grebennikov VV, Beutel RG. 33.  2002. Morphology of the minute larva of Ptinella tenella, with special reference to effects of miniaturisation and the systematic position of Ptiliidae (Coleoptera: Staphylinoidea). Arthropod Struct. Dev. 31:2157–72 [Google Scholar]
  34. Gregory TR. 34.  2001. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. 76:65–101 [Google Scholar]
  35. Hall WE. 35.  1999. Generic revision of the tribe Nanosellini (Coleoptera: Ptiliidae: Ptiliinae). Trans. Am. Entomol. Soc. 125:1/239–126 [Google Scholar]
  36. Hanken J, Wake DB. 36.  1993. Miniaturization of body size: organismal consequences and evolutionary significance. Annu. Rev. Ecol. Syst. 24:501–19Reviews miniaturization in animals (mainly vertebrates). [Google Scholar]
  37. Huber JT. 37.  2000. A new genus of fairyfly, Kikiki, from the Hawaiian Islands (Hymenoptera: Mymaridae). Proc. Hawaii. Entomol. Soc. 34:65–70 [Google Scholar]
  38. Huber JT, Landry J-F. 38.  1999. Cutio nanissimus incredibilis. Nouv'Ailes 9:311 [Google Scholar]
  39. Huber JT, Noyes J. 39.  2013. A new genus and species of fairyfly, Tinkerbella nana (Hymenoptera, Mymaridae), with comments on its sister genus Kikiki, and discussion on small size limits in arthropods. J. Hymenopt. Res. 32:17–44 [Google Scholar]
  40. Hustert R. 40.  2012. Giant and dwarf axons in a miniature insect, Encarsia formosa (Hymenoptera, Calcididae). Arthropod Struct. Dev. 41:6535–43 [Google Scholar]
  41. Ivanova-Kazas OM. 41.  1961. [Essays on the comparative embryology of Hymenoptera] Leningrad: Leningrad Univ. Press
  42. Jackson DJ. 42.  1961. Observations on the biology of Caraphractus cinctus Walker (Hymenoptera, Mymaridae), a parasitoid of the eggs of Dytiscidae. II. Immature stages and seasonal history with a review of mymarid larvae. Parasitology 51:269–94 [Google Scholar]
  43. Kaas JH. 43.  2000. Why is brain size so important: design problems and solutions as neocortex gets bigger or smaller. Brain Mind 1:7–23 [Google Scholar]
  44. Land MF, Nilsson D-E. 44.  2012. Animal Eyes Oxford: Oxford Univ. Press, 2nd ed.. [Google Scholar]
  45. Lin N. 45.  1992. Descriptions of five new species of Megaphragma and Paramegaphragma gen. nov. (Hymenoptera: Trichogrammatidae) from China. Entomotaxonomia 14:2129–38 [Google Scholar]
  46. Makarova AA, Polilov AA. 46.  2013. Peculiarities of the brain organization and fine structure in small insects related to miniaturization. 1. The smallest Coleoptera (Ptiliidae). Entomol. Rev. 93:6703–13 [Google Scholar]
  47. Makarova AA, Polilov AA. 47.  2013. Peculiarities of the brain organization and fine structure in small insects related to miniaturization. 2. The smallest Hymenoptera (Mymaridae, Trichogrammatidae). Entomol. Rev. 93:6714–24 [Google Scholar]
  48. Makarova AA, Polilov AA, Fisher S. 48.  2014. Comparative morphological analysis of compound eye miniaturization in minute Hymenoptera. Arthropod Struct. Dev. In press [Google Scholar]
  49. Mares S, Ash L, Gronenberg W. 49.  2005. Brain allometry in bumblebee and honeybee workers. Brain Behav. Evol. 66:50–61 [Google Scholar]
  50. Martini E. 50.  1912. Studien über die Konstanz histologischer Elemente. III. Hydatina senta. Z. Wiss. Zool. 102:425–645 [Google Scholar]
  51. Matsuda R. 51.  1976. Morphology and Evolution of the Insect Abdomen New York: Pergamon [Google Scholar]
  52. McClain CR, Boyer AG. 52.  2009. Biodiversity and body size are linked across metazoans. Proc. R. Soc. B 276:16652209–15 [Google Scholar]
  53. Meinertzhagen IA. 53.  2010. The organisation of invertebrate brains: cells, synapses and circuits. Acta Zool. Stockholm 91:164–71 [Google Scholar]
  54. Mickoleit E. 54.  1961. Zur Thoraxmorphologie der Thysanoptera. Zool. Jb. Anat. 79:1–92 [Google Scholar]
  55. Mockford EL. 55.  1997. A new species of Dicopomorpha (Hymenoptera: Mymaridae) with diminutive, apterous males. Ann. Entomol. Soc. Am. 90:2115–20Original description of the smallest known insect. [Google Scholar]
  56. Moritz G. 56.  1982. Zur Morphologie und Anatomie des Fransenflüglers Aeolothrips intermedius Bagnall, 1934 (Aeolothripidae, Thysanoptera, Insecta). 3. Mitteilung: Das Abdomen. Zool. Jb. Anat. 108:293–340 [Google Scholar]
  57. Moritz G. 57.  1988. Die Ontogenese der Thysanoptera unter besonderer Berücksichtigung des Fransenflüglers Hercinothrips femoralis (O.M. Reuter 1891). 2. Erst- und Zweitlarve. Zool. Jb. Anat. 117:299–351 [Google Scholar]
  58. Niven JE, Anderson JC, Laughlin SB. 58.  2007. Fly photoreceptors demonstrate energy-information trade-offs in neural coding. PLOS Biol. 5:4e116 [Google Scholar]
  59. Niven JE, Laughlin SB. 59.  2008. Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 211:1792–804 [Google Scholar]
  60. Novotny V, Wilson MR. 60.  1997. Why are there no small species among xylem-sucking insects?. Evol. Ecol. 11:4419–37 [Google Scholar]
  61. Osswald J, Pohl H, Beutel RG. 61.  2010. Extremely miniaturised and highly complex: the thoracic morphology of the first instar larva of Mengenilla chobauti (Insecta, Strepsiptera). Arthropod Struct. Dev. 39:4287–304 [Google Scholar]
  62. Outreman Y, Le Ralec A, Wajnberg E, Pierre JS. 62.  2005. Effects of within- and among-patch experiences on the patch-leaving decision rules in an insect parasitoid. Behav. Ecol. Sociobiol. 58:208–17 [Google Scholar]
  63. Pohl H. 63.  2000. Die Primärlarven der Fächerflügler—evolutionäre Trends (Insecta, Strepsiptera). Kaupia 101–144 [Google Scholar]
  64. Polilov AA. 64.  2005. Anatomy of the feather-winged beetles Acrotrichis montandoni and Ptilium myrmecophilum (Coleoptera, Ptiliidae). Entomol. Rev. 85:5467–75First formulation of hypotheses on limits to insect miniaturization. [Google Scholar]
  65. Polilov AA. 65.  2007. Miniaturization-related structural features of Mymaridae. [Studies on Hymenopterous insects: collection of scientific papers] 50–64 Moscow: KMK [Google Scholar]
  66. Polilov AA. 66.  2008. Anatomy of the smallest of the Coleoptera, feather-winged beetles from tribe Nanosellini (Coleoptera, Ptiliidae) and limits to insect miniaturization. Entomol. Rev. 88:126–33 [Google Scholar]
  67. Polilov AA. 67.  2011. Thoracic musculature of Sericoderus lateralis (Coleoptera, Corylophidae): miniaturization effects and flight muscle degeneration related to development of reproductive system. Entomol. Rev. 91:6735–42 [Google Scholar]
  68. Polilov AA. 68.  2012. The smallest insects evolve anucleate neurons. Arthropod Struct. Dev. 41:127–32 [Google Scholar]
  69. Polilov AA. 69.  2014. Anatomy of Megaphragma, one of the smallest insects (Hymenoptera: Trichogrammatidae) and morphological consequences of miniaturization. Arthropod Struct. Dev. In press [Google Scholar]
  70. Polilov AA. 70.  2014. [Morphological features of the smallest insects]. PhD Thesis, Lomonosov Moscow State Univ., Moscow
  71. Polilov AA, Beutel RG. 71.  2009. Miniaturization effects in larvae and adults of Mikado sp. (Coleoptera: Ptiliidae), one of the smallest free-living insects. Arthropod Struct. Dev. 38:3247–70First complete descriptions of adult and larval morphology and anatomy of some of the smallest insects. [Google Scholar]
  72. Polilov AA, Beutel RG. 72.  2010. Developmental stages of the hooded beetle Sericoderus lateralis (Coleoptera: Corylophidae) with comments on the phylogenetic position and effects of miniaturization. Arthropod Struct. Dev. 39:152–69 [Google Scholar]
  73. Quesada R, Triana E, Vargas G, Douglass JK, Seid MA. 73.  et al. 2011. The allometry of CNS size and consequences of miniaturization in orb-weaving and cleptoparasitic spiders. Arthropod Struct. Dev. 40:6521–29 [Google Scholar]
  74. Rensch B. 74.  1948. Histological changes correlated with evolutionary changes in body size. Evolution 2:218–30First specialized study on effects of size on structure in insects. [Google Scholar]
  75. Riveros AJ, Gronenberg W. 75.  2010. Brain allometry and neural plasticity in the bumblebee Bombus terrestris. Brain Behav. Evol. 75:138–48 [Google Scholar]
  76. Rundell RJ, Leander BS. 76.  2010. Masters of miniaturization: convergent evolution among interstitial eukaryotes. BioEssays 32:5430–37 [Google Scholar]
  77. Schmidt-Nielsen K. 77.  1984. Scaling: Why Is Animal Size So Important? Cambridge: Cambridge Univ. PressPopular monograph on effects of size on animal morphology, physiology, and ecology. [Google Scholar]
  78. Seid MA, Castillo A, Wcislo WT. 78.  2011. The allometry of brain miniaturization in ants. Brain Behav. Evol. 77:15–13 [Google Scholar]
  79. Snodgrass RE. 79.  1926. The morphology of insect sense organs and the sensory nervous system. Smithson. Misc. Coll. 77:81–80 [Google Scholar]
  80. Sorensson M. 80.  1997. Morphological and taxonomical novelties in the world's smallest beetles, and the first Old World records of Nanosellini. Syst. Entomol. 22:257–83 [Google Scholar]
  81. Subba Rao BR. 81.  1969. A new species of Megaphragma (Hymenoptera: Trichogrammatidae) from India. Proc. R. Soc. Lond. B 38:7/8114–16 [Google Scholar]
  82. Swedmark B. 82.  1964. The interstitial fauna of marine sand. Biol. Rev. 39:1–42 [Google Scholar]
  83. Sylvere AP, Stein-Margolina VV. 83.  1976. [Tetrapodili: fore-legs mites; electron microscopic anatomy, evolution problems and mutual relations with plant pathogenic organisms] Tallinn, Estonia: Valgus
  84. Timberlake PH. 84.  1924. Descriptions of new chalcid-flies from Hawaii and Mexico. Proc. Hawaii. Entomol. Soc. 5:395–417 [Google Scholar]
  85. Viggiani G. 85.  1997. Notes on the type of Megaphragma Timberlake (Hymenoptera: Trichogrammatidae), with description of a new species. Boll. Lab. Entomol. Agrar. Filippo Silvestri 53:117–19 [Google Scholar]
  86. Viggiani G, Bernardo U. 86.  1997. Two species of Megaphragma (Hymenoptera Trichogrammatidae), egg-parasitoids of Heliothrips haemorrhoidalis Bouché (Thysanoptera) in southern Italy, with description of a new species. Boll. Zool. Agrar. Bachic. 291:51–55 [Google Scholar]
  87. Warrant EJ, McIntyre PD. 87.  1993. Arthropod eye design and the physical limits to spatial resolving power. Prog. Neurobiol. 40:413–61 [Google Scholar]
  88. Warrant EJ, Nilsson DE. 88.  1998. Absorption of white light in photoreceptors. Vision Res. 38:195–207 [Google Scholar]
  89. Wehner RT, Fukushi T, Isler K. 89.  2007. On being small: brain allometry in ants. Brain Behav. Evol. 69:220–28 [Google Scholar]
  90. White J. 90.  1988. The anatomy. The Nematode Caenorhabditis elegans WB Wood 81–122 Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press [Google Scholar]
  91. Woude E, Smid HM, Chittka L, Huigens ME. 91.  2013. Breaking Haller's rule: brain-body size isometry in a minute parasitic wasp. Brain Behav. Evol. 81:286–92 [Google Scholar]
  92. Yavorskaya MI, Leschen RAB, Polilov AA, Beutel RG. 92.  2014. Unique rostrate larvae and basidiomycophagy in the beetle family Corylophidae. Arthropod Struct. Dev. 43:2153–62 [Google Scholar]
  93. Yavorskaya MI, Polilov AA. 93.  2014. Morphology of the mouthparts of Sericoderus lateralis (Coleoptera, Corylophidae) with comments on effects of the miniaturization. Entomol. Rev. In press [Google Scholar]
/content/journals/10.1146/annurev-ento-010814-020924
Loading
/content/journals/10.1146/annurev-ento-010814-020924
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error