Naturwissenschaften

, Volume 100, Issue 6, pp 581–594

Divergent mating patterns and a unique mode of external sperm transfer in Zoraptera: an enigmatic group of pterygote insects

  • R. Dallai
  • M. Gottardo
  • D. Mercati
  • R. Machida
  • Y. Mashimo
  • Y. Matsumura
  • R. G. Beutel
Original Paper

Abstract

A remarkable external sperm transfer is described for the first time in a species of a group of winged insects (Pterygota), the enigmatic Zoraptera. Mating and sperm transfer of two species of the order were examined in detail, documented, and compared with each other and with patterns described for other species belonging to the order. The behavior differs strikingly in Zorotypus impolitus and Zorotypus magnicaudelli. A copula is performed by males and females of the latter, as it is also the case in other zorapteran species and generally in pterygote insects. In striking contrast to this, males of Z. impolitus do not copulate but deposit small (100 μm in diameter) spermatophores externally on the abdomen of the female. Each spermatophore contains only one giant spermatozoon (3 mm long and 3 μm wide), a unique feature in the entire Hexapoda. External sperm transfer in Pterygota is a highly unusual case of evolutionary reversal. The very small relict group Zoraptera displays a uniform general morphology but exhibits very different reproductive structures and patterns of mating behavior. This may be an extreme form of a more general situation in insects, with a specific form of selection resulting in an accelerated rate of evolution in the reproductive system.

Keywords

Zoraptera Mating behavior Spermatophore Insect reproduction 

Supplementary material

114_2013_1055_MOESM1_ESM.doc (24 kb)
ESM 1Schematic sequences of Zorotypus impolitus mating behavior (DOC 24 kb)
114_2013_1055_MOESM2_ESM.doc (24 kb)
ESM 2Schematic sequences of Zorotypus magnicaudelli mating behavior (DOC 24 kb)
114_2013_1055_MOESM3_ESM.mpg (8.3 mb)
ESM 3Video showing the mating behavior of Zorotypus impolitus (MPG 8460 kb)
114_2013_1055_MOESM4_ESM.mpg (3.6 mb)
ESM 3Video showing the mating behavior of Zorotypus magnicaudelli (MPG 3706 kb)

References

  1. Alberti G (2000) Chelicerata. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates. 9B Oxford and IBH Publishing Co, Queensland, pp 311–388Google Scholar
  2. Alexander RD (1964) The evolution of mating behavior in arthropods. Symp R Entomol Soc Lond 2:78–94Google Scholar
  3. Bareth C (1965) Le spermatophore de Lepidocampa (Diploures Campodéidés). C R Biol 260:3755–3757Google Scholar
  4. Betsch JM (1980) Eléments pour une monographie des Collemboles Symphypléones. Rev Ecol Biol Sol 116A:1–227Google Scholar
  5. Betsch-Pinot MC (1977) Les Parades Sexuelles Primitives Chez Les Collemboles Symphypléones. Rev Ecol Biol Sol 14:15–19Google Scholar
  6. Beutel RG, Weide D (2005) Cephalic anatomy of Zorotypus hubbardi (Hexapoda: Zoraptera): new evidence for a relationship with Acercaria. Zoomorph 124:121–136CrossRefGoogle Scholar
  7. Blancquaert JP, Mertens J (1977) mating behavior in Sphaeridia pumilis (Collembola). Pedobiologia 17:343–349Google Scholar
  8. Blanke A, Wipfler B, Letsch H, Koch M, Beutel R, Misof B (2012) Revival of Palaeoptera—head characters support a monophyletic origin of Odonata and Ephemeroptera (Insecta). Cladistics 28(6):560–581CrossRefGoogle Scholar
  9. Blanke A, Greve C, Wipfler B, Beutel R, Holland B, Misof B (2013) The identification of concerted convergence in insect heads corroborates Palaeoptera. Syst Biol 62(2):250–263PubMedCrossRefGoogle Scholar
  10. Bretfeld G (1970) Grundzüge des Paarungsverhaltens europäischer Bourletiellini (Collembola, Sminthuridae) und daraus abgeleitete taxonomische-nomenklatorische Folgerungen. Z Zool Syst Evol 8:259–273CrossRefGoogle Scholar
  11. Bretfeld G (1977) Der Zyklus von Häutung, Paarung und Eiablage bei den Weibchen von Heterosminthurus insignis (Reuter, 1876) (Collembola, Symphypleona). Rev Ecol BIol Sol 14:1–13Google Scholar
  12. Choe JC (1992) Zoraptera of Panama with a review of the morphology, systematics, and biology of the order. In: Quintero D, Aiello A (eds) Insects of Panama and Mesoamerica: selected studies. Oxford University Press, Oxford, pp 249–256Google Scholar
  13. Choe JC (1994) Sexual selection and mating system in Zorotypus gurneyi Choe (Insecta: Zoraptera): I. Dominance hierarchy and mating success Behav Ecol Sociobiol 34:87–93CrossRefGoogle Scholar
  14. Choe JC (1995) Courtship feeding and repeated mating in Zorotypus barberi (Insecta: Zoraptera). Animal Behav 49(6):1511–1520CrossRefGoogle Scholar
  15. Choe JC (1997) The evolution of mating systems in the Zoraptera: mating variations and sexual conflicts. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 130–145CrossRefGoogle Scholar
  16. Dallai R, Mercati D, Gottardo M, Machida R, Mashimo Y, Beutel RG (2011) The male reproductive system of Zorotypus caudelli Karny (Zoraptera): sperm structure and spermiogenesis. Arthropod Struct Dev 40(6):531–547PubMedCrossRefGoogle Scholar
  17. Dallai R, Mercati D, Gottardo M, Dossey AT, Machida R, Mashimo Y, Beutel RG (2012a) The male and female reproductive systems of Zorotypus hubbardi Caudell, 1918 (Zoraptera). Arthropod Struct Dev 41(4):337–359PubMedCrossRefGoogle Scholar
  18. Dallai R, Mercati D, Gottardo M, Machida R, Mashimo Y, Beutel RG (2012b) The fine structure of the female reproductive system of Zorotypus caudelli Karny (Zoraptera). Arthropod Struct Dev 41(1):51–63PubMedCrossRefGoogle Scholar
  19. Davey KG (1960) The evolution of spermatophores in insects. Proc R Entomol Soc Lond 35:107–13Google Scholar
  20. Dobzhansky TH, Ayala FJ, Stebbins GK, Valentine JW (1977) Evolution. Freeman WH & co, San FranciscoGoogle Scholar
  21. Döring D (1986) On the male reproductive biology of Orchesella cincta (Collembola, Entomobryidae). In: Dallai R (ed) 2nd International Seminar on Apterygota. University of Siena, Siena, pp 171–176Google Scholar
  22. Dybas LK, Dybas HS (1981) Coadaptation and taxonomic differentiation of sperm and spermathecae in featherwing beetles. Evolution 35:168–174CrossRefGoogle Scholar
  23. Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University PressGoogle Scholar
  24. Ehrnsberger R (1977) Fortpflanzungsverhalten der Rhagidiidae (Acarina: Trombidiformes). Acarologia 19:67–73Google Scholar
  25. Ehrnsberger R (1988) Mating behavior of Linopodes sp. (Acariformes: Eupodoidea). In: Channabasavanna GP, Viraktamath CA (eds) Progress in Acarology, vol 1. IBH Publishing Co, Pvt. Ltd. New Delhi, pp 211–218Google Scholar
  26. Engel MS (2003) Phylogeny of the Zoraptera. In Klass KD (ed) Proceedings of the first Dresden meeting on insect phylogeny: “phylogenetic relationships within the insect orders” (Dresden, September 19–21, 2003). Entomol Abh 61(2):147–148Google Scholar
  27. Engel MS, Grimaldi DA (2002) The first Mesozoic Zoraptera (Insecta). Am Mus Novit 3362:1–20CrossRefGoogle Scholar
  28. Ewing HE (1940) The Protura of North America. Ann Entomol Soc Am 33(3):495–551Google Scholar
  29. Fanciulli PP, Zizzari ZV, Frati F, Dallai R (2012) The ultrastructure of the ejaculatory duct in the springtail Orchesella villosa (Geoffroy) (Hexapoda, Collembola) and the formation of the spermatophore. Tissue Cell 44(1):32–46PubMedCrossRefGoogle Scholar
  30. Foelix RF (1992) Biologie der Spinnen, 2nd edn. Thieme, Stuttgart, pp 1–331Google Scholar
  31. Friedrich F, Beutel RG (2008) The thorax of Zorotypus (Hexapoda, Zoraptera) and a new nomenclature for the musculature of Neoptera. Arthropod Struct Dev 37:29–54PubMedCrossRefGoogle Scholar
  32. Gabbutt PD (1954) Notes on the mating behavior of Nemobius sylvestris (Bosc.) (Orth., Gryllidae). Brit J Anim Behav 2(3):84–88CrossRefGoogle Scholar
  33. Grimaldi D, Engel MS (2005) Evolution of the Insects. Cambridge University Press, CambridgeGoogle Scholar
  34. Gurney AB (1938) A synopsis of the order Zoraptera, with notes on the biology of Zorotypus hubbardi Caudell. P Entomol Soc Wash 40:57–87Google Scholar
  35. Gwynne DT (1988) Courtship feeding and the fitness of female katydids (Orthoptera: Tettigoniidae, Requena verticalis). Evolution 42:545–555CrossRefGoogle Scholar
  36. Gwynne DT (1990) The katydid spermatophore: evolution of a parental investment. In: Rentz DC, Bailey W (eds) The biology of Tettigoniidae., pp 27–40CrossRefGoogle Scholar
  37. Gwynne DT, Bowen B, Codd C (1984) The function of the katydid spermatophore and its role in fecundity and insemination (Orthoptera: Tettigoniidae). Aust J Zool 32:15–22CrossRefGoogle Scholar
  38. Higginson DM, Pitnick S (2011) Evolution of intra-ejaculate sperm interactions: do sperm cooperate? Biol Rev Camb Philos Soc 86:249–270PubMedCrossRefGoogle Scholar
  39. Higginson DM, Miller KB, Segraves KA, Pitnick S (2012a) Female reproductive tract form drives the evolution of complex sperm morphology. P Natl Acad Sci USA 109:4538–4543CrossRefGoogle Scholar
  40. Higginson DM, Miller KB, Segraves KA, Pitnick S (2012b) Convergence, recurrence and diversification of complex sperm traits. Evolution 66(5):1650–1661PubMedCrossRefGoogle Scholar
  41. Huber BA (2010) Mating positions and the evolution of asymmetric insect genitalia. Genetica 138(1):19–25PubMedCrossRefGoogle Scholar
  42. Hünefeld F (2007) The genital morphology of Zorotypus hubbardi Caudell, 1918 (Insecta: Zoraptera: Zorotypidae). Zoomorphology 126:135–151CrossRefGoogle Scholar
  43. Hünefeld F, Beutel RG (2005) The sperm pumps of Strepsiptera and Antliophora (Hexapoda). J Zool Syst Evol Res 43(4):297–306CrossRefGoogle Scholar
  44. Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhin S, Birkhead TR (2011) Resolving variation in the reproductive tradeoff between sperm size and number. Proc Nat Acad Sci USA 108(13):5325–5330PubMedCrossRefGoogle Scholar
  45. Jamieson BGM, Dallai R, Afzelius BA (1999) Insects. Their Spermatozoa and Phylogeny. IBH Publishing Ltd., OxfordGoogle Scholar
  46. Janetschek, H (1970) Protura (Beintastler). In: Helmcke JG, Stark D, Wermuth H (eds) Handbuch der Zoologie. Walter de Gruyter & co., Berlin. 4(2) 2/3:1–72Google Scholar
  47. Kaestner A. (1965) Lehrbuch der Speziellen Zoologie, Band I. Wirbellose, 1. Teil, 2. Aufl. Fisher G. StuttgartGoogle Scholar
  48. Kuznetsova VG, Nokkala S, Shcherbakov DE (2002) Karyotype, reproductive organs, and pattern of gametogenesis in Zorotypus hubbardi Caudell (Insecta: Zoraptera, Zorotypidae), with discussion on relationships of the order. Can J Zool 80:1047–1054CrossRefGoogle Scholar
  49. Lewis C, Long TAF (2005) Courtship and reproduction in Carybdea sivickisi (Cnidaria: Cubozoa). Mar Biol 147:477–483CrossRefGoogle Scholar
  50. Mann T (1984) Spermatophores: development, structure, biochemical attributes and role in the transfer of spermatozoa. Springer, New YorkGoogle Scholar
  51. Manton SM (1938) Studies on Onychophora IV. The passage of spermatozoa into the ovary in Peripatopsis Phil Trans R Soc Lond 228:421–442CrossRefGoogle Scholar
  52. Martens J (1978) Spinnentiere, Arachnida. Weberknechte, Opiliones. In: Fischer G (ed) Die Tierwelt Deutschlands. JenaGoogle Scholar
  53. Mashimo Y, Machida R, Dallai R, Gottardo M, Mercati D, Beutel RG (2011) Egg structure of Zorotypus caudelli Karny (Insecta, Zoraptera, Zorotypidae). Tissue Cell 43:230–237PubMedCrossRefGoogle Scholar
  54. Mays DL (1971) Mating behavior of Nemobiine Crickets: Hygronemobius, Nemobius, and Pteronemobius (Orthoptera: Gryllidae). Fla Entomol: 54(2):113–126CrossRefGoogle Scholar
  55. McCartney J, Potter MA, Robertson AW, Telscher K, Lehmann G, Lehmann A, Von-Helversen D, Reinhold K, Achmann R, Heller KG (2008) Understanding nuptial gift size in bush-crickets: an analysis of the genus Poecilimon (Tettigoniidae: Orthoptera). J Orthopt Res 17(2):231–242CrossRefGoogle Scholar
  56. Miller GT, Pitnick S (2002) Sperm-female coevolution in Drosophila. Science 298:1230–1233PubMedCrossRefGoogle Scholar
  57. Minder AM, Hosken DJ, Ward PI (2005) Co-evolution of male and female reproductive characters across the Scathophagidae (Diptera). J Evolution Biol 18:60–69CrossRefGoogle Scholar
  58. Pitnick S, Markow TA (1994) Male gametic strategies: Sperm size, testes size, and the allocation of ejaculate among successive mates by the sperm-limited fly Drosophila pachea and its relatives. Am Nat 143:785–819CrossRefGoogle Scholar
  59. Pitnick S, Markow TA, Spicer GS (1999) Evolution of multiple kinds of female sperm-storage organs in Drosophila Evolution 53:1804–1822Google Scholar
  60. Pitnick S, Hosken DJ, Birkhead T (2009) Sperm morphological diversity. In: Birkhead T, Hosken DJ, Pitnick S (eds) Sperm Biology: An Evolutionary Perspective. Academic, Oxford, pp 69–149CrossRefGoogle Scholar
  61. Proctor HC (1998) Indirect sperm transfer in Arthropods: behavioral and evolutionary trends. Annu Rev Entomol 43:153–74PubMedCrossRefGoogle Scholar
  62. Rugman-Jones PF, Eady PE (2008) Co-evolution of male and female reproductive traits across the Bruchidae (Coleoptera). Funct Ecol 22:880–886CrossRefGoogle Scholar
  63. Schaller F (1971) Indirect sperm transfer by soil arthropods. Annu Rev Entomol 16:407–446CrossRefGoogle Scholar
  64. Schaller F (1979) Significance of sperm transfer and formation of spermatophores in arthropod phylogeny. In: Gupta AP (ed) Arthropod Phylogeny. Van Nostrand Reihold Co, New York-Toronto-London, pp 587–608Google Scholar
  65. Shetlar DJ (1978) Biological observations on Zorotypus hubbardi Caudell (Zoraptera). Entomol News 89:217–223Google Scholar
  66. Silvestri F (1913) Descrizione di un nuovo ordine di insetti. Boll Lab Zool Gen Agrar Portici 7:193–209Google Scholar
  67. Simmons LW, Parker GA (1989) Nuptial Feeding in Insects: Mating Effort versus Paternal Investment. Ethology 81(4):332–343CrossRefGoogle Scholar
  68. Simmons LW, Craig M, Llorens T, Schinzig M, Hosken D (1993) Bushcricket spermatophores vary in accord with sperm competition and parental investment theory. Proc R Soc Lond B 251(1332):183–186CrossRefGoogle Scholar
  69. Sturm H (1978) Zum Paarungsverhalten von Petrobius maritimus Leach (Machilidae: Archaeognatha: Insecta). Zool Anz 201:5–20Google Scholar
  70. Sturm H (1992) Mating behavior and sexual dimorphism in Promesomachilis hispanica Silvestri, 1923 (Machilidae: Archaeognatha: Insecta). Zool Anz 201:5–20Google Scholar
  71. Sturm H, Machida R (2001) Archaeognatha. Handbuch der Zoologie. Walter de Gruyter & co. Berlin 4(37):1–213Google Scholar
  72. Thornhill R (1976) Sexual selection and nuptial feeding behavior in Bittacus apicalis (Insecta: Mecoptera). Am Nat 110:529–548CrossRefGoogle Scholar
  73. Thornhill R, Alcock J (1983) The evolution of Insect mating system. Harvard University Press, CambridgeGoogle Scholar
  74. Trautwein MD, Wiegmann BM, Beutel RG, Kjer KM, Yeates DK (2012) Advances in Insect phylogeny at the dawn of the postgenomic era. Annu Rev Entomol 57:449–468PubMedCrossRefGoogle Scholar
  75. Viscuso R, Brundo MV, Sottile L (2002) Mode of transfer of spermatozoa in Orthoptera Tettigoniidae. Tissue Cell 34:337–348PubMedCrossRefGoogle Scholar
  76. Walker TJ (1978) Post-copulatory behavior of the two-spotted tree cricket, Neoxabea bipunctata. Fla Entomol 61(1):39–40CrossRefGoogle Scholar
  77. Wedell N (1993) Spermatophore size in Bushcrickets: comparative evidence for nuptial gifts as a sperm protection device. Evolution 47(4):1203–1212CrossRefGoogle Scholar
  78. Wedell N (1994) Dual function of the Bushcricket spermatophore. Proc R Soc Lond B 258(1352):181–185CrossRefGoogle Scholar
  79. Weygoldt P (1969) Beobachtungen zur Fortpflanzungsbiologie und zum Verhalten der Geisselspinne Tarantula marginemaculata C.L. Koch (chelicerata, Amblypygi). Z Morphol Ökol Tiere 64:338–360CrossRefGoogle Scholar
  80. Yoshizawa K, Johnson KP (2005) Aligned 18S for Zoraptera (Insecta): phylogenetic position and molecular evolution. Mol Phylogenet Evol 37:572–580PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • R. Dallai
    • 1
  • M. Gottardo
    • 1
  • D. Mercati
    • 1
  • R. Machida
    • 2
  • Y. Mashimo
    • 2
  • Y. Matsumura
    • 3
  • R. G. Beutel
    • 3
  1. 1.Department of Life SciencesSienaItaly
  2. 2.Sugadaira Montane Research CenterUniversity of TsukubaUedaJapan
  3. 3.Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem MuseumFriedrich-Schiller-Universität JenaJenaGermany

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