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Reproductive Anatomy

  • Mamoru Watanabe
Chapter
Part of the Ecological Research Monographs book series (ECOLOGICAL)

Abstract

The reproductive systems of males and females are generally constant in form within butterfly species. Males provide sperm as well as accessory gland substances for transferring to females. During copulation, a single spermatophore including sperm is structured in the bursa copulatrix of females. The bursa copulatrix can contain a full-size spermatophore or remnants of several spermatophores. The sperm to be used for fertilisation is stored in the spermatheca of females, not in the spermatophore. The female oviposition system is essentially a paired structure with two ovaries. Fertilisation takes place in the common oviduct as the sperm pass along this duct and enter the egg. Sperm dimorphism occurs in butterflies. An eupyrene spermatozoon, the normal sperm that can fertilise an egg, is transferred to the female as bundles in the spermatophore. A bundle consists of 256 eupyrene spermatozoa. The apyrene spermatozoon, however, has no nucleus and does not have fertilisation ability. After copulation, both types of spermatozoa move out of the bursa copulatrix, and then arrive at the spermatheca to be stored until oviposition. The spermatheca does not enlarge relative to the stored spermatozoa, suggesting the number of spermatozoa stored is limited. Therefore, the success of sperm migration from the spermatophore to the spermatheca is primarily critical for the reproductive success of the males.

Keywords

Bursa copulatrix Lagena Oviposition Signa Somatic maintenance Spermatheca Spermathecal gland Spermatophore Testes 

References

  1. Ando S, Watanabe M (1992) Egg load and multiple matings of a cabbage butterfly, Pieris canidia indica (Evans), in the wild. Jpn J Appl Entomol Zool 36:200–201. (in Japanese with English summary)CrossRefGoogle Scholar
  2. Ando S, Watanabe M (1993) Mating frequency and egg load in the white butterfly, Pieris melete Menetries, in a wild environment. Jpn J Ecol 43:111–114 (in Japanese)Google Scholar
  3. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton and OxfordCrossRefGoogle Scholar
  4. Boggs CL, Gilbert LE (1979) Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206:83–84CrossRefPubMedGoogle Scholar
  5. Cook PA, Gage MJG (1995) Effects of risks of sperm competition on the numbers of eupyrene and apyrene sperm ejaculated by moth Plodia interpunctella (Lepidoptera: Pyralidae). Behav Ecol Sociobiol 36:261–268CrossRefGoogle Scholar
  6. Cook PA, Wedell N (1999) Non-fertile sperm delay female remating. Nature 397:486CrossRefGoogle Scholar
  7. Drummond BA III (1984) Multiple mating and sperm competition in the Lepidoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, New York, pp 291–370Google Scholar
  8. Dunlap-Pianka H, Boggs CL, Gilbert LE (1977) Ovarian dynamics in heliconiine butterflies: programmed senescence versus eternal youth. Science 197:487–490CrossRefPubMedGoogle Scholar
  9. Elzinga JA, Chevasco V, Grapputo A, Mappes J (2011) Influence of male mating history on female reproductive success among monandrous Naryciinae (Lepidoptera: Psychidae). Ecol Entomol 36:170–180CrossRefGoogle Scholar
  10. Etman AAM, Hooper GHS (1979) Sperm precedence of the last mating in Spodoptera litura. Ann Entomol Soc Am 72:119–120CrossRefGoogle Scholar
  11. Fänger H, Naumann CM (1993) Correlation between the mesodermal male genital ducts and the spermatophore structure in a ditrysian moth, Zygaena trifolii (Esper, 1783) (Insecta, Lepidoptera, Zygaenidae). Acta Zool 74:239–246CrossRefGoogle Scholar
  12. Feltwell J (1986) The natural history of butterflies. Croom Helm, LondonGoogle Scholar
  13. Friedländer M (1997) Control of the eupyrene–apyrene sperm dimorphism in Lepidoptera. J Insect Physiol 43:1085–1092CrossRefPubMedGoogle Scholar
  14. Gage MJG (2012) Complex sperm evolution. Proc Natl Acad Sci USA 109:4341–4342PubMedCentralCrossRefPubMedGoogle Scholar
  15. Gage MJG, Cook PA (1994) Sperm size or numbers? Effects of nutritional stress upon eupyrene and apyrene sperm production strategies in the moth Plodia interpunctella (Lepidoptera: Pyralidae). Funct Ecol 8:594–599CrossRefGoogle Scholar
  16. Galicia I, Sánchez V, Cordero C (2008) On the function of signa, a genital trait of female Lepidoptera. Ann Entomol Soc Am 101:786–793CrossRefGoogle Scholar
  17. He Y, Tanaka T, Miyata T (1995) Eupyrene and apyrene sperm and their numerical fluctuations inside the female reproductive tract of the armyworm, Pseudaletia separata. J Insect Physiol 41:689–694CrossRefGoogle Scholar
  18. Hiroyoshi S, Mitsuhashi J (1999) Sperm reflux and its role in multiple mating in males of a butterfly Polygonia c-aureum Linnaeus (Lepidoptera: Nymphalidae). J Insect Physiol 45:107–112CrossRefPubMedGoogle Scholar
  19. Katsuno S (1977) Studies on eupyrene and apyrene spermatozoa in the silk worm, Bombyx mori L. (Lepidoptera: Bombycidae). II. The intratesticular behaviour of the spermatozoa after emergence. Appl Entomol Zool 12:236–240Google Scholar
  20. Konagaya T, Mutoh N, Suzuki M, Rutowski RL, Watanabe M (2015) Estimates of female lifetime fecundity and changes in the number and types of sperm stored with age and time since mating in the monandrous swallowtail butterfly, Battus philenor (Lepidoptera: Papilionidae) in the Arizona desert. Appl Entomol Zool 50:311–316CrossRefGoogle Scholar
  21. Labine PA (1966) The population biology of the butterfly, Euphydryas editha. IV. Sperm precedence: a preliminary report. Evolution 20:580–586CrossRefGoogle Scholar
  22. LaChance LE, Richard RD, Ruud RL (1977) Movement of eupyrene sperm bundles from the testis and storage in the ductus ejaculatoris duplex of the male pink bollworm: effects of age, strain, irradiation, and light. Ann Entomol Soc Am 70:647–651CrossRefGoogle Scholar
  23. LaMunyon CW, Eisner T (1993) Postcopulatory sexual selection in an arctiid moth (Utetheisa ornatrix). Proc Natl Acad Sci USA 90:4689–4692PubMedCentralCrossRefPubMedGoogle Scholar
  24. Lewis Z, Wedell N (2009) Male moths reduce sperm investment in relatives. Anim Behav 77:1547–1550CrossRefGoogle Scholar
  25. Lincango P, Fernández G, Baixeras J (2013) Microstructure and diversity of the bursa copulatrix wall in Tortricidae (Lepidoptera). Arthropod Struct Dev 42:247–256CrossRefPubMedGoogle Scholar
  26. Mancini K, Dolder H (2001) Ultrastructure of apyrene and eupyrene spermatozoa from the seminal vesicle of Euptoieta hegesia (Lepidoptera: Nymphalidae). Tissue Cell 33:301–308CrossRefPubMedGoogle Scholar
  27. Nabi MN, Harrison RA (1983) Activity of sperm and fertility in the potato moth, Phthorimaea operculella. J Insect Physiol 29:431–435CrossRefGoogle Scholar
  28. Nakanishi Y, Watanabe M, Ito T (1996) Differences in lifetime reproductive output and mating frequency of two female morphs of the sulfur butterfly, Colias erate (Lepidoptera: Pieridae). J Res Lepid 35:1–8CrossRefGoogle Scholar
  29. Norris MJ (1936) The feeding-habits of the adult Lepidoptera Heteroneura. Trans R Entomol Soc Lond 85:61–90CrossRefGoogle Scholar
  30. Porter K (1992) Eggs and egg-laying. In: Dennis RLH (ed) The ecology of butterflies in Britain. Oxford University Press, Oxford, pp 46–72Google Scholar
  31. Riemann JG, Thorson BJ, Ruud RL (1974) Daily cycle of release of sperm from the testes of the Mediterranean flour moth. J Insect Physiol 20:195–207CrossRefGoogle Scholar
  32. Rutowski RL (1984) Sexual selection and the evolution of butterfly mating behavior. J Res Lepid 23:125–142Google Scholar
  33. Sahara K, Takemura Y (2003) Application of artificial insemination technique to eupyrene and/or apyrene sperm in Bombyx mori. J Exp Zool A 297:196–200CrossRefGoogle Scholar
  34. Sánchez V, Hernández-Baños BE, Cordero C (2011) The evolution of a female genital trait widely distributed in the Lepidoptera: comparative evidence for an effect of sexual coevolution. PLoS ONE 6:e22642PubMedCentralCrossRefPubMedGoogle Scholar
  35. Sasaki N, Watanabe M (2015) Alternative ejaculate allocation tactics in relation to male mating history of the swallowtail butterfly, Papilio xuthus L. (Lepidoptera: Papilionidae). J Res Lepid 48:1–8Google Scholar
  36. Sasaki N, Konagaya T, Watanabe M, Rutowski RL (2015) Indicators of recent mating success in the pipevine swallowtail butterfly (Battus philenor) and their relationship to male phenotype. J Insect Physiol 83:30–36CrossRefPubMedGoogle Scholar
  37. Shepherd JG (1974) Activation of saturniid moth sperm by a secretion of the male reproductive tract. J Insect Physiol 20:2107–2122CrossRefPubMedGoogle Scholar
  38. Silberglied RE, Shepherd JG, Dickinson JL (1984) Eunuchs: the role of apyrene sperm in Lepidoptera? Am Nat 123:255–265CrossRefGoogle Scholar
  39. Sugawara T (1979) Stretch reception in the bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behaviour. J Comp Physiol 130:191–199CrossRefGoogle Scholar
  40. Suzuki N, Okuda T, Shinbo H (1996) Sperm precedence and sperm movement under different copulation intervals in the silkworm, Bombyx mori. J Insect Physiol 42:199–204CrossRefGoogle Scholar
  41. Swallow JG, Wilkinson GS (2002) The long and short of sperm polymorphisms in insects. Biol Rev 77:153–182CrossRefPubMedGoogle Scholar
  42. Tschudi-Rein K, Benz G (1990) Mechanisms of sperm transfer in female Pieris brassicae (Lepidoptera: Pieridae). Ann Entomol Soc Am 83:1158–1164CrossRefGoogle Scholar
  43. Tsukaguchi R, Kurotsu T (1922) On the apyrene spermatozoa of the Lepidoptera. Zool Mag 34:310–317 (in Japanese)Google Scholar
  44. Watanabe M (1981) Population dynamics of the swallowtail butterfly, Papilio xuthus L., in a deforested area. Res Popul Ecol 23:74–93CrossRefGoogle Scholar
  45. Watanabe M (1988) Multiple matings increase the fecundity of the yellow swallowtail butterfly, Papilio xuthus L., in summer generations. J Insect Behav 1:17–29CrossRefGoogle Scholar
  46. Watanabe M (1992) Egg maturation in laboratory-reared females of the swallowtail butterfly, Papilio xuthus L. (Lepidoptera: Papilionidae), feeding on different concentration solutions of sugar. Zool Sci 9:133–141Google Scholar
  47. Watanabe M, Ando S (1993) Influence of mating frequency of lifetime fecundity in wild females of the small white Pieris rapae (Lepidoptera, Pieridae). Jpn J Entomol 61:691–696Google Scholar
  48. Watanabe M, Ando S (1994) Egg load in wild females of the small white Pieris rapae crucivora (Lepidoptera, Pieridae) in relation to mating frequency. Jpn J Entomol 62:293–297Google Scholar
  49. Watanabe M, Hachisuka A (2005) Dynamics of eupyrene and apyrene sperm storage in ovipositing females of the swallowtail butterfly Papilio xuthus (Lepidoptera: Papilionidae). Entomol Sci 8:65–71CrossRefGoogle Scholar
  50. Watanabe M, Hirota M (1999) Effects of sucrose intake on spermatophore mass produced by male swallowtail butterfly Papilio xuthus L. Zool Sci 16:55–61CrossRefGoogle Scholar
  51. Watanabe M, Kobayashi T (2006) Total sperm ejaculation in monandrous (Papilio machaon) and polyandrous (P. xuthus) swallowtail butterflies (Lepidoptera: Papilionidae) restricted to larval stage-derived nutrients. J Res Lepid 39:1–7Google Scholar
  52. Watanabe M, Nishimura M (2001) Reproductive output and egg maturation in relation to mate-avoidance in monandrous females of the small copper, Lycaena phlaeas (Lycaenidae). J Lepid Soc 54:83–87Google Scholar
  53. Watanabe M, Nozato K (1986) Fecundity of the yellow swallowtail butterflies, Papilio xuthus and P. machaon hippocrates, in a wild environment. Zool Sci 3:509–516Google Scholar
  54. Watanabe M, Sasaki N (2010) Pattern of sperm storage and migration in the reproductive tract of the swallowtail butterfly Papilio xuthus: cryptic female choice after second mating. Physiol Entomol 35:328–333CrossRefGoogle Scholar
  55. Watanabe M, Sato K (1993) A spermatophore structured in the bursa copulatrix of the small white Pieris rapae (Lepidoptera, Pieridae) during copulation and its sugar content. J Res Lepid 32:26–36Google Scholar
  56. Watanabe M, Nozato K, Kiritani K (1986) Studies on ecology and behavior of Japanese black swallowtail butterflies (Lepidoptera: Papilionidae). 5. Fecundity in summer generations. Appl Entomol Zool 21:448–453Google Scholar
  57. Watanabe M, Wiklund C, Bon’no M (1998) The effect of repeated matings on sperm numbers in successive ejaculates of the cabbage white butterfly Pieris rapae (Lepidoptera: Pieridae). J Insect Behav 11:559–570CrossRefGoogle Scholar
  58. Watanabe M, Bon’no M, Hachisuka A (2000) Eupyrene sperm migrates to spermatheca after apyrene sperm in the swallowtail butterfly, Papilio xuthus L. (Lepidoptera: Papilionidae). J Ethol 18:91–99CrossRefGoogle Scholar
  59. Wedell N, Cook PA (1999) Strategic sperm allocation in the small white butterfly Pieris rapae (Lepidoptera: Pieridae). Funct Ecol 13:85–93CrossRefGoogle Scholar
  60. Wickman P-O (1985) Male determined mating duration in butterflies? J Lepid Soc 39:341–342Google Scholar
  61. Yamagishi M, Ito Y, Tsubaki Y (1992) Sperm competition in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae): effects of sperm “longevity” on sperm precedence. J Insect Behav 5:599–608CrossRefGoogle Scholar
  62. Yan S, Li H, Zhang J, Zhu J, Zhang Q, Liu X (2013) Sperm storage and sperm competition in the Helicoverpa armigera (Lepidoptera: Noctuidae). J Econ Entomol 106:708–715CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  • Mamoru Watanabe
    • 1
  1. 1.Graduate School of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan

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