This comprehensive review of the structure of sperm in all orders of insects evaluates phylogenetic implications, with the background of a phylogeny based on transcriptomes. Sperm characters strongly support several major branches of the phylogeny of insects—for instance, Cercophora, Dicondylia, and Psocodea—and also different infraordinal groups. Some closely related taxa, such as Trichoptera and Lepidoptera (Amphiesmenoptera), differ greatly in sperm structure. Sperm characters are very conservative in some groups (Heteroptera, Odonata) but highly variable in others, including Zoraptera, a small and morphologically uniform group with a tremendously accelerated rate of sperm evolution. Unusual patterns such as sperm dimorphism, the formation of bundles, or aflagellate and immotile sperm have evolved independently in several groups.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Afzelius BA, Dallai R. 1.  1994. Characteristics of the flagellar axoneme of Neuroptera, Coleoptera, and Strepsiptera. J. Morphol. 219:15–20 [Google Scholar]
  2. Alves L, Mancini K, Lino-Neto J, Dolder H. 2.  2006. Morphology of the male reproductive system and sperm ultrastructure of Leucoptera coffeella (Lepidoptera: Lyonetiidae). Acta Zool. 87:131–39 [Google Scholar]
  3. Araújo VA, Lino-Neto J, Ramalho FS, Zanuncio JC, Serrão JE. 3.  2011. Ultrastructure and heteromorphism of spermatozoa in five species of bugs (Pentatomidae: Heteroptera). Micron 42:560–67 [Google Scholar]
  4. Araújo VA, Moreira J, Lino-Neto J. 4.  2009. Structure and ultrastructure of the spermatozoa of Trypoxylon (Trypargilum) albitarse Fabricius 1804 (Hymenoptera: Apoidea: Crabronidae). Micron 40:719–23 [Google Scholar]
  5. Aspöck U, Plant JD, Nemeschkal HL. 5.  2001. Cladistic analysis of Neuroptera and their systematic position within Neuropterida (Insecta: Holometabola: Neuropterida: Neuroptera). Syst. Entomol. 26:73–86 [Google Scholar]
  6. Baccetti B. 6.  1987. Spermatozoa and phylogeny in orthopteroid insects. Evolutionary Biology of Orthopteroid Insects B Baccetti 12–112 Chichester, UK: Horwood [Google Scholar]
  7. Baccetti B, Burrini AG, Dallai R, Pallini V. 7.  1982. A motile system of singlet microtubules in spermatozoa. Cell Motil. Cytoskelet. 2:93–101 [Google Scholar]
  8. Baccetti B, Dallai R. 8.  1977. The spermatozoon of Arthropoda. XXIX. The degenerated axoneme and branched acrosome of aleyrodids. J. Ultrastruct. Res. 61:260–70 [Google Scholar]
  9. Baccetti B, Dallai R, Burrini AG. 9.  1973. The spermatozoon of Arthropoda. XVIII. The non-motile bifurcated sperm of Psychodidae flies. J. Cell Sci. 12:287–311 [Google Scholar]
  10. Baccetti B, Dallai R, Callaini G. 10.  1981. The spermatozoon of Arthropoda: Zootermopsis nevadensis and isopteran sperm phylogeny. Int. J. Invertebr. Reprod. 3:87–89 [Google Scholar]
  11. Baccetti B, Dallai R, Giusti F, Bernini F. 11.  1974. The spermatozoon of Arthropoda. XXIII. The “9+9+3” spermatozoon of simuliid diptera. J. Ultrastruct. Res. 46:427–40 [Google Scholar]
  12. Baccetti B, Dallai R, Pallini V, Rosati F, Afzelius BA. 12.  1977. Protein of insect sperm mitochondrial crystals: Crystallomitin. J. Cell Biol. 73:594–600 [Google Scholar]
  13. Baccetti B, Dallai R, Rosati F. 13.  1969. The spermatozoon of Arthropoda III. The lowest holometabolic insects. J. Microsc. 8:233–48 [Google Scholar]
  14. Baccetti B, Dallai R, Rosati F. 14.  1969. The spermatozoon of Arthropoda. IV. Corrodentia, Mallophaga and Thysanoptera. J. Microsc. 8:249–62 [Google Scholar]
  15. Baccetti B, De Coninck E. 15.  1989. Immotile, aflagellate spermatozoa in Ptiliidae coleopterans. Biol. Cell 67:185–91 [Google Scholar]
  16. Báo SN, Kitajima EW, Callaini G, Lupetti P, Dallai R. 16.  1997. Spermiogenesis in three species of whiteflies (Homoptera, Aleyrodidae). Acta Zool. 78:163–70 [Google Scholar]
  17. Beutel RG, Friedrich F, Ge SQ, Yang XK. 17.  2013. Insect Morphology and Phylogeny Berlin: De GruyterThe state of the art in insect morphology and an overview of morphological features and phylogenetic relationships of the hexapod orders.
  18. Beutel RG, Friedrich F, Hörnschemeyer T, Pohl H, Hünefeld F. 18.  et al. 2011. Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola. Cladistics 27:341–55 [Google Scholar]
  19. Beutel RG, Gorb SN. 19.  2006. A revised interpretation of the evolution of attachment structures in Hexapoda with special emphasis on Mantophasmatodea. Arthropod Syst. Phylogeny. 64:3–25 [Google Scholar]
  20. Birkhead TR, Hosken DJ, Pitnick S. 20.  2009. Sperm Biology: An Evolutionary Perspective Oxford, UK: AcademicProvides a synthesis on sperm morphology, sperm competition, and speciation in different groups of animals.
  21. Blanke A, Greve C, Wipfler B, Beutel R, Holland B, Misof B. 21.  2012. The identification of concerted convergence in insect heads corroborates Palaeoptera. Syst. Biol. 162:250–63 [Google Scholar]
  22. Blanke A, Wipfler B, Letsch H, Koch M, Beckmann F. 22.  et al. 2012. Revival of Palaeoptera—head characters support a monophyletic origin of Odonata and Ephemeroptera (Insecta). Cladistics 28:560–81 [Google Scholar]
  23. Boudreaux HB. 23.  1979. Arthropod Phylogeny with Special Reference to Insects New York: Wiley
  24. Burrini AG, Magnano L, Magnano AR, Scala C, Baccetti B. 24.  1988. Spermatozoa and phylogeny of Curculionidea. Int. J. Insect Morphol. Embryol. 17:1–50 [Google Scholar]
  25. Cruz-Landim C, Kitajima EW. 25.  1972. The ultrastructure of male spermatozoa of corn leafhopper Dalbulus maidis Del. and W. (Homoptera: Cicadellidae). J. Submicrosc. Cytol. 4:75–82 [Google Scholar]
  26. Cryan JR, Urban JM. 26.  2012. Higher-level phylogeny of the insect order Hemiptera: Is Auchenorrhyncha really paraphyletic?. Syst. Ent. 37:7–21 [Google Scholar]
  27. Dallai R. 27.  1972. The arthropod spermatozoon. XVII. Machilis distincta Janetsch (Insecta Thysanura). Monit. Zool. Ital. 6:37–61 [Google Scholar]
  28. Dallai R. 28.  1979. An overview of atypical spermatozoa in insects. The Spermatozoon DW Fawcett, JM Bedford 253–65 Baltimore, MD: Urban Schawarzenberg [Google Scholar]
  29. Dallai R. 29.  2014. Overview on spermatogenesis and sperm structure of Hexapoda. Arthropod Struct. Dev. 43:257–90Gives a broad and detailed overview of spermatogenesis and structural features of spermatozoa in Hexapoda. [Google Scholar]
  30. Dallai R, Afzelius BA. 30.  1985. Membrane specializations in the paired spermatozoa of dytiscid water beetle. Tissue Cell 17:561–72 [Google Scholar]
  31. Dallai R, Afzelius BA. 31.  1990. Microtubular diversity in insect spermatozoa: results obtained with a new fixative. J. Struct. Biol. 103:164–79 [Google Scholar]
  32. Dallai R, Afzelius BA. 32.  1990. Ultrastructural patterns of the flagellar axoneme in the non-motile part of the mole-cricket sperm. Biol. Cell 70:19–26 [Google Scholar]
  33. Dallai R, Afzelius BA. 33.  1991. Sperm flagellum of insects belonging to insect orders of Psocoptera, Mallophaga and Anoplura: ultrastructural and phylogenetic aspects. Boll. Zool. 58:211–16 [Google Scholar]
  34. Dallai R, Afzelius BA. 34.  1994. Sperm structure of Trichoptera. I. Integripalpia: Limnephiloidea. Int. J. Insect Morphol. Embryol. 23:197–209 [Google Scholar]
  35. Dallai R, Afzelius BA. 35.  1995. Sperm structure in Trichoptera. II. The aflagellate spermatozoa of Hydroptila, Orthotrichia and Stactobia (Hydroptilidae). Int. J. Insect Morphol. Embryol. 24:161–70 [Google Scholar]
  36. Dallai R, Afzelius BA. 36.  1999. Accessory microtubules in insect spermatozoa: structure, function and phylogenetic significance. The Male Gamete: From Basic Science to Clinical Applications C Cagnon 333–50 Vienna, IL: Cache River [Google Scholar]
  37. Dallai R, Afzelius BA, Lupetti P, Osella G. 37.  1998. Sperm structure of some Curculionoidea and their relationship with Chrysomeloidea. Boll. Mus. Regionale Sci. Nat. Torino. 1:27–50 [Google Scholar]
  38. Dallai R, Baccetti B, Mazzini M, Sabatinelli G. 38.  1984. The spermatozoon of three species of Phlebotomus (Phlebotomidae) and the acrosomal evolution in nematoceran dipterans. Int. J. Insect Morphol. Embryol. 13:1–10 [Google Scholar]
  39. Dallai R, Beani L, Kathirithamby J, Lupetti P, Afzelius BA. 39.  2003. New findings on sperm ultrastructure of Xenos vesparum (Rossi) (Strepsiptera, Insecta). Tissue Cell 35:19–27 [Google Scholar]
  40. Dallai R, Bellon PL, Lanzavecchia S, Afzelius BA. 40.  1993. The dipteran sperm tail: ultrastructural characteristics and phylogenetic considerations. Zool. Scr. 22:193–202 [Google Scholar]
  41. Dallai R, Frati F, Lupetti P, Adis J. 41.  2003. Sperm ultrastructure of Mantophasma zephyra (Insecta, Mantophasmatodea). Zoomorphology 122:67–76 [Google Scholar]
  42. Dallai R, Gottardo M, Mercati D, Machida R, Mashimo Y. 42.  et al. 2013. Divergent mating patterns and a unique mode of external sperm transfer in Zoraptera: an enigmatic group of pterygote insects. Naturwissenschaften 100:581–94 [Google Scholar]
  43. Dallai R, Gottardo M, Mercati D, Machida R, Mashimo Y. 43.  et al. 2014. Comparative morphology of spermatozoa and reproductive systems of zorapteran species from different world regions (Insecta, Zoraptera). Arthropod Struct. Dev. 43:371–83 [Google Scholar]
  44. Dallai R, Gottardo M, Mercati D, Machida R, Mashimo Y. 44.  et al. 2014. Giant spermatozoa and a huge spermatheca: a case of coevolution of male and female reproductive organs in the ground louse Zorotypus impolitus (Insecta, Zoraptera). Arthropod Struct. Dev. 43:135–51 [Google Scholar]
  45. Dallai R, Gottardo M, Mercati D, Rafael JA, Machida R. 45.  et al. 2015. The intermediate sperm type and genitalia of Zorotypus shannoni Gurney: evidence supporting infraordinal lineages in Zoraptera (Insecta). Zoomorphology 134:79–91 [Google Scholar]
  46. Dallai R, Lupetti P, Afzelius BA, Frati F. 46.  2003. Sperm structure of Mecoptera and Siphonaptera (Insecta) and the phylogenetic position of Boreus hyemalis. Zoomorphology 122:211–20 [Google Scholar]
  47. Dallai R, Lupetti P, Afzelius BA. 47.  1995. Sperm structure of Trichoptera. III. Hydropsychidae, Polycentropodidae and Philopotamidae (Annulipalpia). Int. J. Insect Morphol. Embryol. 24:171–83 [Google Scholar]
  48. Dallai R, Lupetti P, Afzelius BA. 48.  1995. Sperm structure of Trichoptera. IV. Rhyacophilidae and Glossosomatidae. Int. J. Insect Morphol. Embryol. 24:185–93 [Google Scholar]
  49. Dallai R, Lupetti P, Afzelius BA, Mamaev BM. 49.  1995. Characteristics of the sperm flagellum in fungus gnats (Mycetophiloidea, Diptera, Insecta). Zoomorphology 115:213–19 [Google Scholar]
  50. Dallai R, Lupetti P, Frati F, Nardi F, Afzelius BA. 50.  2001. Binucleate and biflagellate spermatozoa in Tricholepidion gertschi Wygodzinsky (Insecta, Zygentoma). Tissue Cell 33:606–13 [Google Scholar]
  51. Dallai R, Lupetti P, Mencarelli C. 51.  2006. Unusual axonemes of hexapod spermatozoa. Int. Rev. Cytol. 254:45–99 [Google Scholar]
  52. Dallai R, Lupetti P, Osella G, Afzelius BA. 52.  2005. Giant sperm with accessory macrotubules in a neuropteran insect. Tissue Cell 37:359–66 [Google Scholar]
  53. Dallai R, Machida R, Jintsu Y, Frati F, Lupetti P. 53.  2007. The sperm structure of Embioptera (Insecta) and phylogenetic considerations. Zoomorphology 126:53–59 [Google Scholar]
  54. Dallai R, Machida R, Uchifune T, Lupetti P, Frati F. 54.  2005. The sperm structure of Galloisiana yuasai (Insecta, Grylloblattodea) and implications for the phylogenetic position of Grylloblattodea. Zoomorphology 124:205–12 [Google Scholar]
  55. Dallai R, Mercati D, Carapelli C, Nardi F, Machida R. 55.  et al. 2011. Sperm accessory microtubules suggest the placement of Diplura as the sister-group of Insecta s.s. Arthropod Struct. Dev. 40:77–92 [Google Scholar]
  56. Dallai R, Mercati D, Gottardo M, Dossey AT, Machida R. 56.  et al. 2012. The male and female reproductive systems of Zorotypus hubbardi Caudell, 1918 (Zoraptera). Arthropod Struct. Dev. 41:337–59 [Google Scholar]
  57. Dallai R, Mercati D, Gottardo M, Machida R, Mashimo Y, Beutel RG. 57.  2011. The male reproductive system of Zorotypus caudelli Karny (Zoraptera): sperm structure and spermiogenesis. Arthropod Struct. Dev. 40:531–47 [Google Scholar]
  58. Dallai R, Mercati D, Gottardo M, Machida R, Mashimo Y, Beutel RG. 58.  2012. The fine structure of the female reproductive system of Zorotypus caudelli Karny (Zoraptera). Arthropod Struct. Dev. 41:51–63 [Google Scholar]
  59. Dallai R, Thipaksorn A, Gottardo M, Mercati D, Machida R, Beutel RG. 59.  2015. The sperm structure of Cryptocercus punctulatus Scudder (Blattodea) and sperm evolution in Dictyoptera. J. Morphol. 276:361–69 [Google Scholar]
  60. Dallai R, Zizzari ZV, Fanciulli PP. 60.  2008. Fine structure of the spermatheca and of the accessory glands in Orchesella villosa (Collembola, Hexapoda). J. Morphol. 269:464–78 [Google Scholar]
  61. Dallai R, Zizzari ZV, Fanciulli PP. 61.  2008. The ultrastructure of the spermathecae in the Collembola Symphypleona (Hexapoda). J. Morphol. 269:1122–33 [Google Scholar]
  62. Drummond BA. 62.  1984. Multiple mating and sperm competition in the Lepidoptera. Sperm Competition and the Evolution of Animal Mating Systems RL Smith 291–370 London: Academic [Google Scholar]
  63. Fausto AM, Belardinelli M, Fochetti R, Mazzini M. 63.  2001. Comparative spermatology in Plecoptera (Insecta): an ultrastructural investigation on four species. Arthropod Struct. Dev. 30:55–62 [Google Scholar]
  64. Fausto AM, Belardinelli M, Fochetti R, Tierno de Figueroa JM, Mazzini M. 64.  2002. Comparative spermatology in Plecoptera (Insecta). II. An ultrastructural investigation on four species of Systellognatha. Arthropod Struct. Dev. 31:147–56 [Google Scholar]
  65. Fausto AM, Mazzini M, Maroli M, Feliciangeli MD. 65.  1995. Spermatozoon of the sandfly Lutzomyia longipalpis (Lutz and Neiva) (Diptera, Psychodidae). Boll. Zool. 62:339–43 [Google Scholar]
  66. Folliot R, Maillet P. 66.  1970. Ultrastructure de la spermiogenèse et du spermatozoïde de divers insectes Homoptères. Comparative Spermatology B Baccetti 289–300 New York: Academic [Google Scholar]
  67. Friedemann K, Spangenberg R, Yoshizawa K, Beutel RG. 67.  2013. The evolution of attachment structures in the highly diverse Acercaria (Hexapoda). Cladistics 30:70–201 [Google Scholar]
  68. Friedländer M. 68.  1983. Phylogenetic branching of Trichoptera and Lepidoptera: an ultrastructural analysis on comparative spermatology. J. Ultrastruct. Res. 83:141–47 [Google Scholar]
  69. Friedländer M, Morse JC. 69.  1982. The aberrant spermatozoa of Hydropsychidae caddisflies (Trichoptera). J. Ultrastruct. Res. 78:84–94 [Google Scholar]
  70. Friedländer M, Seth RK, Reynolds SE. 70.  2005. Eupyrene and apyrene sperm: dichotomous spermatogenesis in Lepidoptera. Advances in Insect Physiology 32 S Simpson 206–308 Oxford, UK: Elsevier [Google Scholar]
  71. Gaino E, Mazzini M. 71.  1991. Aflagellate sperm in three species of Leptophlebiidae (Ephemeroptera). Int. J. Insect Morphol. Embryol. 20:119–25 [Google Scholar]
  72. Gottardo M, Mercati D, Dallai R. 72.  2012. The spermatogenesis and sperm structure of Timema poppensis (Insecta: Phasmatodea). Zoomorphology 131:209–23 [Google Scholar]
  73. Grimaldi DA, Engel MS. 73.  2005. Evolution of the Insects Cambridge, UK: Cambridge Univ. Press
  74. Hamon C, Chauvin G. 74.  1992. Ultrastructural analysis of spermatozoa of Korscheltellus lupinus L. (Lepidoptera, Hepialidae) and Micropterix calthella L. (Lepidoptera, Micropterigidae). Int. J. Insect Morphol. Embryol. 21:149–60 [Google Scholar]
  75. Hennig W. 75.  1969. Die Stammesgeschichte der Insekten Frankfurt am Main, Germ.: Waldemar KramerThis book is a milestone in insect systematics, based on a strictly phylogenetic concept for the first time.
  76. Higginson DM, Miller KB, Segraves KA, Pitnick S. 76.  2012. Convergence, recurrence and diversification of complex sperm traits in diving beetles (Dytiscidae). Evolution 66:1650–61 [Google Scholar]
  77. Higginson DM, Pitnick S. 77.  2011. Evolution of intra-ejaculate sperm interactions: Do sperm cooperate?. Biol. Rev. 86:249–70 [Google Scholar]
  78. Hünefeld F, Beutel RG. 78.  2005. The sperm pumps of Strepsiptera and Antliophora (Hexapoda). J. Zool. Syst. Evol. Res. 43:297–306 [Google Scholar]
  79. Inward D, Beccaloni G, Eggleton P. 79.  2007. Death of an order: A comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol. Lett. 3:331–35 [Google Scholar]
  80. Ito S. 80.  1966. Movement and structure of louse spermatozoa. J. Cell Biol. 31:128a [Google Scholar]
  81. Jamieson BGM, Dallai R, Afzelius BA. 81.  1999. Insects: Their Spermatozoa and Phylogeny Enfield, NH: ScienceA comprehensive overview of the sperm structure in the hexapod orders.
  82. Katsuno S. 82.  1978. Studies on eupyrene and apyrene spermatozoa in the silk-worm, Bombyx mori (Lepidoptera: Bombycidae) L. VII. The motility of sperm bundles and spermatozoa in the reproductive organs of males and females. Appl. Entomol. Zool. 13:91–96 [Google Scholar]
  83. King PE, Ahmed KS. 83.  1989. Sperm structure in Psocoptera. Acta Zool. 70:57–61 [Google Scholar]
  84. Klass KD, Zompro O, Kristensen NP, Adis J. 84.  2002. Mantophasmatodea: a new insect order with extant members in the Afrotropics. Science 296:1456–59 [Google Scholar]
  85. Kristensen NP. 85.  1991. Phylogeny of extant hexapods. The Insects of Australia: A Textbook for Students and Research Workers CSIRO 125–40 Melbourne, Aust.: Melbourne Univ. Press [Google Scholar]
  86. Kristensen NP. 86.  1997. The groundplan and basal diversification of the hexapods. Arthropod Relationships RA Fortey, RH Thomas 281–93 London: Chapman Hall [Google Scholar]
  87. Kukalová-Peck J. 87.  1991. Fossil history and the evolution of hexapod structures. The Insects of Australia: A Textbook for Students and Researchers CSIRO 141–79 Melbourne, Aust.: Melbourne Univ. Press [Google Scholar]
  88. Le Menn R. 88.  1966. Observation sur la spermiogenèse et le spermatozoïde del Psyllides (Homoptera, Psylloidea). C. R. Acad. Sci. Paris Ser. D 262:1730–36 [Google Scholar]
  89. Lino-Neto J, Báo SN, Dolder H. 89.  1999. Structure and ultrastructure of the spermatozoa of Bephratelloides pomorum (Fabricius) (Hymenoptera: Eurytomidae). Int. J. Insect Morphol. Embryol. 28:253–59 [Google Scholar]
  90. Lino-Neto J, Báo SN, Dolder H. 90.  2000. Sperm ultrastructure of the honey bee (Apis mellifera) (L.) (Hymenoptera, Apidae) with emphasis on the nucleus-flagellum transition region. Tissue Cell 32:322–27 [Google Scholar]
  91. Lino-Neto J, Dolder H. 91.  2001. Redescription of sperm structure and ultrastructure of Trichogramma dendrolimi (Hymenoptera: Chalcidoidea: Trichogrammatidae). Acta Zool. 82:159–64 [Google Scholar]
  92. Lino-Neto J, Dolder H. 92.  2001. Ultrastructural characteristics of the spermatozoa of Scelionidae (Hymenoptera, Platygastroidea) with phylogenetic considerations. Zool Scr. 30:89–96 [Google Scholar]
  93. Lino-Neto J, Dolder H, Mancini K, Mercati D, Dallai R. 93.  2008. The short spermatodesm of Arge pagana (Hymenoptera: Symphyta). Tissue Cell 40:185–93 [Google Scholar]
  94. Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M. 94.  et al. 2000. Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr. Biol. 10:801–4 [Google Scholar]
  95. Lupetti P, Mencarelli C, Mercati D, Gaino E, Dallai R. 95.  2011. The spermatodesm of Cloeon dipterum (L.): fine structure and sperm movement. Tissue Cell 43:157–64 [Google Scholar]
  96. Lupetti P, Mercati D, Dallai R. 96.  2001. The sperm glycocalyx of Pezzotettix giornai (Rossi) (Insecta: Orthoptera) after quick-freeze, deep-etching. Ital. J. Anat. Embryol 106:Suppl. 2181–88 [Google Scholar]
  97. Mashimo Y, Beutel RG, Dallai R, Lee C-Y, Machida R. 97.  2013. Embryonic development of Zoraptera with special reference to external morphology, and its phylogenetic implications (Insecta). J. Morphol. 275:295–312 [Google Scholar]
  98. Mazzini M. 98.  1970. Lo spermatozoo di un afide: Megoura viciae Kalt. Atti Accad. Sci. Siena Fisiocrit. 14:21–6 [Google Scholar]
  99. Mazzini M. 99.  1976. Giant spermatozoa in Divales bipustulatus F. (Coleoptera: Cleridae). Int. J. Insect Morphol. Embryol. 5:107–15 [Google Scholar]
  100. Mazzini M, Carcupino M, Kathirithamby J. 100.  1991. Fine structure of the spermatozoon of the strepsipteran Xenos moutoni. Tissue Cell 23:199–207 [Google Scholar]
  101. Mazzini M, Fausto AM, Maroli M. 101.  1992. Fine structure of the spermatozoon of the sandfly Sergentomyia minuta (Diptera, Psychodidae). Boll. Zool. 59:343–47 [Google Scholar]
  102. Mencarelli C, Mercati D, Dallai R, Lupetti P. 102.  2014. Ultrastructure of the sperm axoneme and molecular analysis of axonemal dynein in Ephemeroptera (Insecta). Cytoskeleton 71:328–39 [Google Scholar]
  103. Mercati D, Giusti F, Dallai R. 103.  2009. A novel membrane specialization in the sperm tail of bug insects (Heteroptera). J. Morphol. 270:825–33 [Google Scholar]
  104. Misof B, Liu S, Meusemann K, Peters RS, Donath A. 104.  et al. 2014. Phylogenomics resolves the timing pattern of insect evolution. Science 346:763–67A recent phylogeny of all Hexapoda based on 1,478 orthologous genes, the largest molecular data set ever used in insect systematics. [Google Scholar]
  105. Moreira J, Araújo VA, Lino-Neto J. 105.  2012. Morphological aspects of testes and sperm ultrastructure in the “symphyta” Digelasinus diversipes Kirby 1882 (Hymenoptera: Argidae: Dielocerinae). Microsc. Res. Tech. 75:609–14 [Google Scholar]
  106. Moreira J, Zama U, Lino-Neto J. 106.  2004. Release, behavior and phylogenetic significance of spermatozoa in bundles in the seminal vesicles during sexual maturation in Aculeata (Hymenoptera). J. Morphol. Sci. 21:145–52 [Google Scholar]
  107. Morrow EH. 107.  2004. How the sperm lost its tail: the evolution of aflagellate sperm. Biol. Rev. 79:795–814 [Google Scholar]
  108. Nardi JB, Delgado JA, Collantes F, Miller LA, Bee CM, Kathirithamby J. 108.  2013. Sperm cells of a primitive Strepsipteran. Insects 4:463–75 [Google Scholar]
  109. Niehuis O, Hartig G, Grath S, Pohl H, Lehmann J. 109.  et al. 2012. Genomic and morphological evidence converge to resolve the enigma of Strepsiptera. Curr. Biol. 22:1309–13 [Google Scholar]
  110. Paccagnini E, Lupetti P, Afzelius BA, Dallai R. 110.  2009. New findings on sperm ultrastructure in thrips (Thysanoptera, Insecta). Arthropod Struct. Dev. 38:70–83 [Google Scholar]
  111. Paccagnini E, Mencarelli C, Mercati D, Afzelius BA, Dallai R. 111.  2007. Ultrastructural analysis of the aberrant axoneme morphogenesis in thrips (Thysanoptera, Insecta). Cell Motil. Cytoskelet. 64:645–61 [Google Scholar]
  112. Paccagnini E, Mercati D, Giusti F, Conti B, Dallai R. 112.  2010. The spermatogenesis and the sperm structure of Terebrantia (Thysanoptera, Insecta). Tissue Cell 42:247–58 [Google Scholar]
  113. Paoli F, Gottardo M, Dallai R, Roversi PF. 113.  2013. Morphology of the male reproductive system and sperm ultrastructure of the egg parasitoid Gryon pennsylvaticum (Ashmead) (Hymenoptera, Platygastridae). Arthropod Struct. Dev. 42:297–308 [Google Scholar]
  114. Peters RS, Meusemann K, Petersen M, Wilbrandt J, Ziesmann J. 114.  et al. 2014. The evolutionary history of holometabolous insects inferred from transcriptome-based phylogeny and comprehensive morphological data. BMC Evol. Biol. 14:52 [Google Scholar]
  115. Phillips DM. 115.  1966. Fine structure of Sciara coprophila sperm. J. Cell Biol. 30:499–517 [Google Scholar]
  116. Phillips DM. 116.  1969. Exceptions to the prevailing pattern of tubules (9+9+2) in the sperm flagella of certain insect species. J. Cell Biol. 40:28–43 [Google Scholar]
  117. Phillips DM. 117.  1970. Insect sperm: their structure and morphogenesis. J. Cell Biol. 44:243–77 [Google Scholar]
  118. Phillips DM. 118.  1971. Insect flagellar tubule patterns. Theme and variations. Comparative Spermatology B Baccetti 263–73 New York: Academic [Google Scholar]
  119. Pohl H, Dallai R, Gottardo M, Beutel RG. 119.  2013. The spermatozoon of Mengenilla moldrzyki (Strepsiptera, Mengenillidae): ultrastructure and phylogenetic considerations. Tissue Cell 45:397–401 [Google Scholar]
  120. Quicke DLJ, Ingram SN, Baillie HS, Gaitens PV. 120.  1992. Sperm structure and ultrastructure in the Hymenoptera (Insecta). Zool. Scr. 21:381–402 [Google Scholar]
  121. Reumont BM, Jenner RA, Wills MA, Dell'Ampio E, Pass G. 121.  et al. 2012. Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda. Mol. Biol. Evol. 29:1031–45 [Google Scholar]
  122. Riparbelli MG, Callaini G, Mercati D, Hertel H, Dallai R. 122.  2009. Centrioles to basal bodies in the spermiogenesis of Mastotermes darwiniensis (Insecta, Isopoda). Cell Motil. Cytoskelet. 66:1100–5 [Google Scholar]
  123. Robison WG. 123.  1972. Microtubular patterns in spermatozoa of coccid insects in relation to bending. J. Cell Biol. 52:66–83 [Google Scholar]
  124. Russell LK, Dallai R, Gottardo M, Beutel RG. 124.  2013. The sperm ultrastructure of Caurinus dectes Russell (Mecoptera: Boreidae) and its phylogenetic implications. Tissue Cell 45:397–401 [Google Scholar]
  125. Santos HP, Zama U, Dolder H, Lino-Neto J. 125.  2013. Sperm morphology of Trichospilus diatraeae and Palmistichus elaeisis (Hymenoptera: Chalcidoidea: Eulophidae). Micron 51:36–40 [Google Scholar]
  126. Silberglied RE, Shepherd JG, Dickinson JL. 126.  1984. Eunuchs: the role of apyrene sperm in Lepidoptera?. Am. Nat. 123:255–65 [Google Scholar]
  127. Sivinsky J. 127.  1984. Sperm in competition. Sperm Competition and the Evolution of Animal Mating Systems RL Smith 86–115 San Diego, CA: Academic [Google Scholar]
  128. Snook RR. 128.  1997. Is the production of multiple sperm types adaptive?. Evolution 51:797–808 [Google Scholar]
  129. Sonnenschein M, Häuser CL. 129.  1990. Presence of only eupyrene spermatozoa in adult males of the genus Micropteryx Hübner and its phylogenetic significance. Int. J. Insect Morphol. Embryol. 19:269–76 [Google Scholar]
  130. Staniczek AH. 130.  2000. The mandible of silverfish (Insecta: Zygentoma) and mayflies (Ephemeroptera): its morphology and phylogenetic significance. Zool. Anzeiger 239:147–78 [Google Scholar]
  131. Terry MD, Whiting MF. 131.  2005. Mantophasmatodea and phylogeny of the lower neopterous insects. Cladistics 21:240–57 [Google Scholar]
  132. Werner G. 132.  1965. Untersuchungen Über Die Spermiogenese Beim Sandläufer, Cicindela campestris L. Z. Zellforch. Mikrosk. Anat. Abt. Histochem 66:255–75 [Google Scholar]
  133. White MJD. 133.  1973. The evolution of aberrant genetic systems. Animal Cytology and Evolution MJD White 500–46 Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  134. Wiegmann BM, Trautwein MD, Kim JW, Cassel BK, Bertone MA. 134.  et al. 2009. Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol. 7:34 [Google Scholar]
  135. Wilkes A, Lee PE. 135.  1965. The ultrastructure of dimorphic spermatozoa in the hymenopteran Dahlbominus fuscipennis (Zett.) Eulophidae. Can. J. Genet. Cytol. 7:609–19 [Google Scholar]
  136. Wingstrand KG. 136.  1972. Comparative Spermatology of a Pentastomid, Raillietiella hemidactyli, and a Branchiuran Crustacean, Argulus foliaceus, with a Discussion of Pentastomid Relationships Copenhagen: Munksgaard [Google Scholar]
  137. Wingstrand KG. 137.  1973. The spermatozoa of the thysanuran insects Petrobius brevistylus Carp. and Lepisma saccharina L. Acta Zool. 54:31–52 [Google Scholar]
  138. Wipfler B, Machida R, Müller B, Beutel RG. 138.  2011. On the head morphology of Grylloblattodea (Insecta) and the systematic position of the order, with a new nomenclature for the head muscles of Neoptera. Syst. Entomol. 36:241–66 [Google Scholar]
  139. Yoshizawa K, Johnson KP. 139.  2003. Phylogenetic position of Phthiraptera (Insecta: Paraneoptera) and elevated rate of evolution in mitochondrial 12S and 16S rDNA. Mol. Phylogenetics Evol. 29:102–14 [Google Scholar]
  140. Yoshizawa K, Johnson KP. 140.  2010. How stable is the “Polyphyly of Lice” hypothesis (Insecta: Psocodea)? A comparision of phylogenetic signal in multiple genes. Mol. Phylogenetics Evol. 55:939–51 [Google Scholar]
  141. Yoshizawa K, Saigusa T. 141.  2001. Phylogenetic analysis of paraneopteran orders (Insecta: Neoptera) based on forewing base structure, with comments on monophyly of Auchenorrhyncha (Hemiptera). Syst. Entomol. 26:1–13 [Google Scholar]
  142. Zagrodzinska B, Dallai R. 142.  1988. Spermiogenesis in the gall-midge Monarthropalpus buxi (Cecidomyiidae, Diptera). J. Ultrastruct. Mol. Struct. Res. 100:156–65 [Google Scholar]
  143. Zhang B, Hua B. 143.  2014. Sperm ultrastructure of Panorpodes kuandianensis (Mecoptera, Panorpidae). Microsc. Res. Tech. 77:394–400 [Google Scholar]
  144. Zizzari ZV, Lupetti P, Mencarelli C, Dallai R. 144.  2008. Sperm ultrastructure and spermiogenesis of Coniopterygidae (Neuroptera, Insecta). Arthropod Struct. Dev. 37:410–17 [Google Scholar]
  145. Zizzari ZV, Lupetti P, Pantaleoni RA, Letardi A, Dallai R. 145.  2011. Sperm structure of some Neuroptera and phylogenetic considerations. Ital. J. Zool. 78:35–44 [Google Scholar]
  146. Zizzari ZV, Machida R, Tsutsumi K, Reynoso-Velasco D, Lupetti P, Dallai R. 146.  2010. Ultrastructural studies on euspermatozoa and paraspermatozoa in Mantispidae (Insecta, Neuroptera). Tissue Cell 42:81–87 [Google Scholar]
  147. Zylberberg L. 147.  1969. Contribution a l'étude de la double spermatogenèse chez un lépidoptère (Pieris brassicae L, Pieridae). Ann. Sci. Nat. Zool. 11:569–626 [Google Scholar]

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