Two intromittent organs in Zorotypus caudelli (Insecta, Zoraptera): The paradoxical coexistence of an extremely long tube and a large spermatophore

Biological Journal of the Linnean Society

Volumn 112, Issue 1, 2014, Pages 40-54

  Matsumura, Yoko ^a   Yoshizawa, Kazunori ^b   Machida, Ryuichiro ^c   Mashimo, Yuta ^c   Dallai, Romano ^d   Gottardo, Marco ^d   Kleinteich, Thomas ^e   Michels, Jan ^e   Gorb, Stanislav N ^e   Beutel, Rolf G ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

^d UNIVERSITY OF SIENA   (Italy)

^e UNIVERSITY OF KIEL   (Germany)

Author keywords

Copulation; Insertion; Novelty; Penis; Preadaptation; Sexual selection; Withdrawal

Indexed keywords

HEXAPODA; INSECTA; ZORAPTERA; ZOROTYPUS;

EID: 84898849624     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/bij.12260     Document Type: Article

References (53)

1. Alexander RD, Otte D. 1967. The evolution of genitalia and mating behaviour in crickets (Gryllidae). Miscellaneous Publications Museum of Zoology University of Michigan 133: 1-62.
2. Anthes N, Michiels NK. 2007a. Precopulatory stabbing, hypodermic injections and unilateral copulations in a hermaphroditic sea slug. Biology Letters 3: 121-124.
3. Anthes N, Michiels NK. 2007b. Reproductive morphology, mating behavior, and spawning ecology of cephalaspid sea slugs (Aglajidae and Gastropteridae). Invertebrate Biology 126: 335-365.
4. Aspöck U, Aspöck H. 2008. Phylogenetic relevance of the genital sclerites of Neuropterida (Insecta: Holometabola). Systematic Entomology 33: 97-127.
5. Beutel RG, Weide D. 2005. Cephalic anatomy of Zorotypus hubbardi (Hexapoda: Zoraptera): new evidence for a relationship with Acercaria. Zoomorphology 124: 121-136.
6. Bolivar y Pieltain C. 1940. Estudio de un Nuevo Zoráptero de México. Anales de la Escuela Nacional de Ciencias Biológicas 1: 515-523.
7. Bragg PE. 1991. Spermatophores in Phasmida. Entomologist 110: 76-80.
8. Briceño RD, Orozco D, Quintero JL, Hanson P, Hernández MDR. 2011. Copulatory behaviour and the process of intromission in Anastrepha ludens (Diptera: Tephritidae). Revista de Biologia Tropical 59: 291-297.
9. Chapman RF. 1998. The insects: structure and function. Cambridge: Cambridge University Press.
10. Choe JC. 1995. Courtship feeding and repeated mating in Zorotypus barberi (Insecta: Zoraptera). Animal Behaviour 49: 1511-1520.
11. Dallai R, Del Bene G, Lupetti P. 1997. Fine structure of the male reproductive organs of the western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). International Journal of Insect Morphology and Embryology 26: 97-112.
12. Dallai R, Gottardo M, Mercati D, Machida R, Mashimo Y, Matsumura Y, Beutel RG. 2013. Divergent mating patterns and a unique mode of external sperm transfer in Zoraptera: an enigmatic group of pterygote insects. Naturwissenschaften 100: 581-594.
13. Dallai R, Gottardo M, Mercati D, Machida R, Mashimo Y, Matsumura Y, Beutel RG. 2014a. 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 Structure & Development 43: 135-151.
14. Dallai R, Gottardo M, Mercati D, Machida R, Mashimo Y, Matsumura Y, Rafael JA, Beutel RG. 2014b. Comparative morphology of spermatozoa and reproductive systems of zorapteran species from different world regions (Insecta, Zoraptera). Arthropod Structure & Development (in press).
15. 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 Structure & Development 40: 531-547.
16. 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 Structure & Development 41: 337-359.
17. 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 Structure & Development 41: 51-63.
18. Eberhard WG. 1985. Sexual selection and animal genitalia. Cambridge, MA: Harvard University Press.
19. Eberhard WG. 1996. Female control: sexual selection by cryptic female choice. Princeton, NJ: Princeton University Press.
20. Eberhard WG. 2005. Threading a needle with reinforced thread: intromission in Ceratitis capitata (Diptera, Tephritidae). The Canadian Entomologist 137: 174-181.
21. Eberhard WG, Pereira F. 1995. The process of intromission in the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidiae). Psyche 102: 99-120.
22. Friedrich F, Beutel RG. 2008. Micro-computer tomography and a renaissance of insect morphology. Proceedings of SPIE 7048: 1-6.
23. Gack C, Peschke K. 2005. 'Shouldering' exaggerated genitalia: a unique behavioural adaptation for the retraction of the elongate intromittant organ by the male rove beetle (Aleochara tristis Gravenhorst). Biological Journal of the Linnean Society 84: 307-312.
24. Gschwentner R, Tadler A. 2000. Functional anatomy of the spermatheca and its duct in the seed bug Lygaeus simulans (Heteroptera: Lygaeidae). European Journal of Entomology 97: 305-312.
25. Gurney AB. 1938. A synopsis of the order Zoraptera, with notes on the biology of Zorotypus hubbardi Caudell. Proceedings of the Entomological Society of Washington 40: 57-87.
26. Holwell GI. 2007. Spermatophore feeding and mating behaviour in praying mantids (Mantodea: Liturgusidae). Journal of Zoology 271: 255-260.
27. Hünefeld F. 2007. The genital morphology of Zorotypus hubbardi Caudell, 1918 (Insecta: Zoraptera: Zorotypidae). Zoomorphology 126: 135-151.
28. Kamimura Y. 2000. Possible removal of rival sperm by the elongated genitalia of the earwig, Euborellia plebeja. Zoological Science 17: 667-672.
29. Kamimura Y. 2005. Last-male paternity of Euborellia plebeja, an earwig with elongated genitalia and sperm removal behavior. Journal of Ethology 23: 35-41.
30. Koene JM, Chiba S. 2006. The way of the samurai snail. American Naturalist 168: 553-555.
31. Lange R, Werminghausen J, Anthes N. 2014. Cephalo-traumatic secretion transfer in a hermaphrodite sea slug. Proceedings of the Royal Society of London Series B, Biological Sciences 281: 20132424.
32. van Lieshout E, Elgar MA. 2011. Longer exaggerated male genitalia confer defensive sperm-competitive benefits in an earwig. Evolutionary Ecology 25: 351-362.
33. Marchini D, del Bene G, Falso LF, Dallai R. 2001. Structural organization of the copulatory site in the medfly Ceratitis capitata (Diptera: Tephritidae) and observations on sperm transfer and storage. Arthropod Structure & Development 30: 39-54.
34. Mashimo Y, Machida R, Dallai R, Gottardo M, Mercati D, Beutel RG. 2011. Egg structure of Zorotypus caudelli Karny (Insecta, Zoraptera, Zorotypidae). Tissue and Cell 43: 230-237.
35. Mashimo Y, Yoshizawa K, Engel MS, Ghani IAB, Dallai R, Beutel RG, Machida R. 2013. Zorotypus in Peninsular Malaysia (Zoraptera: Zorotypidae), with the description of three new species. Zootaxa 3717: 498-514.
36. Matsumura Y, Yoshizawa K. 2010. Insertion and withdrawal of extremely elongated genitalia: a simple mechanism with a highly modified morphology in the leaf beetle, Lema coronata. Biological Journal of the Linnean Society 99: 512-520.
37. Matsumura Y, Yoshizawa K. 2012. Homology of the internal sac components in the leaf beetle subfamily Criocerinae and evolutionary novelties related to the extremely elongated flagellum. Journal of Morphology 273: 507-518.
38. Michels J, Gorb SN. 2012. Detailed three-dimensional visualization of resilin in the exoskeleton of arthropods using confocal laser scanning microscopy. Journal of Microscopy 245: 1-16.
39. New TR. 1978. Notes on Neotropical Zoraptera, with descriptions of two new species. Systematic Entomology 3: 361-370.
40. New TR. 2000. Zoraptera (Insecta) in east Malaysia: notes on Zorotypus caudelli Karny. Oriental Insects 34: 77-82.
41. Pohl H. 2010. A scanning electron microscopy specimen holder for viewing different angles of a single specimen. Microscopy Research and Technique 73: 1073-1076.
42. Proctor HC. 1998. Indirect sperm transfer in arthropods: behavioral and evolutionary trends. Annual Review of Entomology 43: 153-174.
43. Rodriguez V. 1994. Function of the spermathecal muscle in Chelymorpha alternans Boheman (Coleoptera: Chrysomelidae: Cassidinae). Physiological Entomology 19: 198-202.
44. Rodriguez V. 1995. Copulatory courtship in Chelymorpha alternans Boheman (Coleoptera: Chrysomelidae: Cassidinae). The Coleopterists Bulletin 49: 327-331.
45. Rodriguez V, Windsor D, Eberhard WG. 2004. Tortoise beetle genitalia and demonstration of a selected advantage for flagellum length in Cherymorpha alternans (Chrysomelidae, Cassidini, Stolaini. In: Jolivet P, Santiago-Blay JA, Schmitt M, eds. New developments in the biology of Chrysomelidae. The Hague: SBP Academic Publisher, 739-748.
46. Ross ES. 1970. Biosystematics of the Embioptera. Annual Review of Entomology 15: 157-172.
47. Snodgrass RE. 1935. Principles of insect morphology. New York, NY: McGraw-Hill Book Co..
48. Spencer KA. 1981. A revisionary study of the leaf mining flies (Agromyzidae) of California. Berkeley, CA: Division of Agricultural Sciences, University of California, Special Publication.
49. Tadler A. 1999. Selection of a conspicuous male genitalic trait in the seedbug Lygaeus simulans. Proceedings of the Royal Society of London Series B, Biological Sciences 266: 1773-1777.
50. Thornhill R. 1983. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. American Naturalist 122: 765-788.
51. Verma KK, Kumar D. 1972. The aedeagus, its musculature, and 'retournement' in Aspidomorpha miliaris F. (Coleoptera, Phytophaga, Chrysomelidae). Journal of Natural History 6: 699-719.
52. Villavaso EJ. 1975. Function of the spermathecal muscle in the boll weevil, Anthonomus grandis. Journal of Insect Physiology 21: 1275-1278.
53. Yoshizawa K. 2011. Monophyletic Polyneoptera recovered by wing base structure. Systematic Entomology 36: 377-394.