Eur. J. Entomol. 107 (1): 55-59, 2010 | DOI: 10.14411/eje.2010.006

Speed or sperm: A potential trade-off between development and reproduction in the butterfly, Bicyclus anynana (Lepidoptera: Nymphalidae)

Zenobia LEWIS1, Paul M. BRAKEFIELD2, Nina WEDELL3
1 Graduate School of Environmental Science, Okayama University, Okayama 700-0084, Japan; e-mail: zen.lewis@gmail.com
2 Institute of Biology, Leiden University, PO Box 9505, 2300 RA Leiden, The Netherlands; e-mail: p.m.brakefield@biology.leidenuniv.nl
3 Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Tremough, Penryn, Cornwall, TR10 9EZ, UK; e-mail: n.wedell@exeter.ac.uk

Life-history theory predicts trade-offs between resources invested in reproduction and other fitness-related traits. To date, most studies have focused on potential reproductive trade-offs in females. However, it is now generally accepted that reproduction is also costly for males, and thus males too may be subject to trade-offs. We examined the relationship between development time and the production of both fertile and non-fertile sperm in males of the African bush brown butterfly (Bicyclus anynana) selected for short or long pre-adult development time. Fast developing males ejaculated fewer non-fertile sperm on their first mating, suggesting that there could be a trade-off between ejaculate production and development time in this species. Contrary to predictions, slow developing males were smaller, produced fewer fertile sperm and took longer to mate. We discuss why this might be the case, and suggest that there may be a cost to the production of non-fertile sperm in the Lepidoptera.

Keywords: Lepidoptera, Nymphalidae, Bicyclus anynana, reproduction, trade-off, development time, polymorphic sperm

Received: June 11, 2009; Revised: October 6, 2009; Accepted: October 6, 2009; Published: February 15, 2010  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
LEWIS, Z., BRAKEFIELD, P.M., & WEDELL, N. (2010). Speed or sperm: A potential trade-off between development and reproduction in the butterfly, Bicyclus anynana (Lepidoptera: Nymphalidae). EJE107(1), 55-59. doi: 10.14411/eje.2010.006
Download citation

References

  1. BATEMAN A.J. 1948: Intrasexual selection in Drosophila. Heredity 2: 349-368 Go to original source...
  2. BENREY B. & DENNO R.F. 1997: The slow-growth-high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78: 987-999 Go to original source...
  3. BISSOONDATH C.J. & WIKLUND C. 1996: Effect of male mating history and body size on ejaculate size and quality in two polyandrous butterflies, Pieris napi and Pieris rapae (Lepidoptera: Pieridae). Funct. Ecol. 10: 457-464 Go to original source...
  4. BRAKEFIELD P.M. & REITSMA N. 1991: Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol. Entomol. 16: 291-303 Go to original source...
  5. BRAKEFIELD P.M., EL FILALI E., VAN DER LAAN R., BREUKER C.J., SACCHERI I.J. & ZWAAN B.J. 2001: Effective population size, reproductive success and sperm precedence in the butterfly, Bicyclus anynana, in captivity. J. Evol. Biol. 14: 148-156 Go to original source...
  6. BREUKER C.J. & BRAKEFIELD P.M. 2002: Female choice depends on size but not symmetry of dorsal eyespots in the butterfly Bicyclus anynana. Proc. R. Soc. Lond. (B) 269: 1233-1239 Go to original source...
  7. CHAPMAN T., MIYATAKE T., SMITH H.K. & PARTRIDGE L. 1998: Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly, Ceratitis capitata. Proc. R. Soc. Lond. (B) 265: 1879-1894 Go to original source...
  8. COOK P.A. & WEDELL N. 1996: Ejaculate dynamics in butterflies: A strategy for maximizing fertilization success? Proc. R. Soc. Lond. (B) 263: 1047-1051 Go to original source...
  9. COOK P.A. & WEDELL N. 1999: Non-fertile sperm delay female remating. Nature 397: 486-486 Go to original source...
  10. DRUMMOND B. 1984: Multiple mating and sperm competition in the Lepidoptera. In Smith R.L. (ed.): Sperm Competition and the Evolution of Animal Mating Systems. Academic Press, London, pp. 291-370 Go to original source...
  11. FISCHER K., ZWAAN B.J. & BRAKEFIELD P.M. 2007: Realized correlated responses to artificial selection on pre-adult lifehistory traits in a butterfly. Heredity 98: 157-164 Go to original source...
  12. FRIEDLANDER M. 1997: Control of the eupyrene-apyrene dimorphism in Lepidoptera. J. Insect Physiol. 43: 1085-1092 Go to original source...
  13. GAGE M.J.G. & COOK P.A. 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: 594-599 Go to original source...
  14. GIEBULTOWICZ J.M., BELL R.A. & IMBERSKI R.B. 1988: Circadian rhythm of sperm movement in the male reproductive tract of the gypsy moth, Lymantria dispar. J. Insect Physiol. 34: 527-532 Go to original source...
  15. GOTTHARD K. 2000: Increased risk of predation as a cost of high growth rate: an experimental test in a butterfly. J. Anim. Ecol. 69: 896-902 Go to original source...
  16. GOTTHARD K., NYLIN S. & WIKLUND C. 1994: Adaptive variation in growth rate - life history costs and consequences in the speckled wood butterfly, Pararge aegeria. Oecologia 99: 281-289 Go to original source...
  17. GURDON G.B. 1991: Nuclear transplantation in Xenopus. In Kray B. & Peng B. (eds): Methods in Cell Biology. London Academic Press, London, pp. 299-306 Go to original source...
  18. JERVIS M.A., BOGGS C.L. & FERNS P.N. 2005: Egg maturation and its associated trade-offs: a synthesis focusing on Lepidoptera. Ecol. Entomol. 30: 359-375 Go to original source...
  19. JORON M. & BRAKEFIELD P.M. 2003: Captivity masks inbreeding effects on male mating success in butterflies. Nature 424: 191-194 Go to original source...
  20. KAITALA A. & WIKLUND C. 1995: Female mate choice and mating costs in the polyandrous butterfly Pieris rapi (Lepidoptera, Pieridae). J. Insect Behav. 8: 355-363 Go to original source...
  21. LEWIS Z. & WEDELL N. 2007: Effect of adult diet on male mating behavior in the butterfly, Bicyclus anynana (Lepidoptera, Nymphalidae). J. Insect Behav. 20: 201-213 Go to original source...
  22. MEVES F. 1902: Uber oligopyrene und apyrene spermien und ueber ihre entstehung, nach beobachtungen an Paludina und Pygaera. Arch. Mikrosk. Anat. 61: 1-84 Go to original source...
  23. MUKAI T. & YAMAZAKI T. 1971: The genetic structure of natural populations of Drosophila melanogaster. X. Developmental time and viability. Genetics 69: 385-398 Go to original source...
  24. PIJPE J., FISCHER K., BRAKEFIELD P.M. & ZWAAN B.J. 2006: Consequences of artificial selection on pre-adult development for adult lifespan under benign conditions in the butterfly Bicyclus anynana. Mech. Ageing Dev. 127: 802-807 Go to original source...
  25. ROFF D.A. 1992: The Evolution of Life Histories. Chapman and Hall, New York, 552 pp
  26. ROFF D.A. 2002: Life History Evolution. Sinauer Associates, Sunderland, MA, 527 pp
  27. SACCHERI I.J., LLYOD H.D., HELYAR S.J. & BRAKEFIELD P.M. 2005: Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly. Proc. R. Soc. Lond. (B) 272: 39-46 Go to original source...
  28. SILBERGLIED R.E., SHEPHERD J.G. & DICKINSON J.L. 1984: Eunuchs: the role of apyrene sperm in Lepidoptera? Am. Nat. 123: 255-265 Go to original source...
  29. WEDELL N. 2005: Female receptivity in butterflies. J. Exp. Biol. 208: 3433-3440 Go to original source...
  30. WEDELL N. & COOK P.A. 1998: Determinants of paternity in a butterfly. Proc. R. Soc. Lond. (B) 265: 625-630 Go to original source...
  31. WEDELL N., GAGE M.J.G. & PARKER G.A. 2002: Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17: 313-320 Go to original source...
  32. WIKLUND C. & FAGERSTROM T. 1977: Why do males emerge before females? A hypothesis to explain the incidence of protandry in butterflies. Oecologia 31: 153-158 Go to original source...
  33. ZIJLSTRA W.G., ZWAAN B.J. & BRAKEFIELD P.M. 2001: Bad cold for a butterfly? Proc. Sec. Exp. Appl. Entomol. Netherl. Entomol. Soc. 12: 19-23
  34. ZIJLSTRA W.G., KESBECKE F., ZWAAN B.J. & BRAKEFIELD P.M. 2002: Protandry in the butterfly Bicyclus anynana. Evol. Ecol. Res. 4: 1229-1240
  35. ZWAAN B.J., ZIJLSTRA W.G., KELLER M., PIJPE J. & BRAKEFIELD P.M. 2008: Potential constraints on evolution: sexual dimorphism and the problem of protandry in the butterfly Bicyclus anynana. J. Genet. 87: 395-405 Go to original source...

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.