Behavioral Ecology and Sociobiology

, Volume 33, Issue 1, pp 25–33

Polyandry and its effect on female reproduction in the green-veined white butterfly (Pieris napi L.)

  • Christer Wiklund
  • Arja Kaitala
  • Virpi Lindfors
  • Johan Abenius


In many insects nutrients transferred by the male to the female at mating are later incorporated into both the eggs and soma of the mated females. Accordingly, it has been suggested that female insects can use these male-derived nutrients both for somatic maintenance and to increase both the number and quality of their offspring. Moreover, much discussion is presently devoted to whether the male nuptial gift represents paternal investment, defined as “any increase in given male's total surviving progeny by increasing the reproductive output by a given female”, or mating effort which obtains “if a male gains by increasing the proportion of eggs he fertilizes from a given female” (Parker and Simmons 1989). If the male nuptial gift represents parental investment it should be expected to benefit predominantly the offspring sired by the donor, whereas the “physiological fate” of the male nuptial gift is somewhat irrelevant under the mating effort explanation. In this paper we test these issues by studying the lifetime fecundity, egg weights and longevity of two groups of females of the polyandrous green-veined white butterfly, Pieris napi, one group of which was allowed to mate only once and the other of which was allowed to mate at liberty, the latter group of females mating on average 2.28 times. Moreover, to test the incorporation rate of male-derived nutrients, we performed a second set of experiments where females were allowed to mate with radioactively labelled males. The results showed that polyandrous females had higher lifetime fecundity compared to monandrous females, laying on average 1.61 as many eggs, and that the difference in cumulative fecundity between the two groups was statistically significant from the 5th day of egg-laying onwards. Polyandrous females also lived longer and maintained egg weight at a high level for longer than monandrous females. Largely concomitant with egg-laying rate, incorporation rate of male-derived nutrients peaked 3–4 days after mating, subsequently tapering off to stabilize at about 40% of the maximum. Given the opportunity, female P. napi remated after 3–5 days, the duration of the refractory period being positively correlated with ejaculate mass. Hence, although the nutrient investment of the first male to mate with a female “subsidizes” the progeny of later-mating males, the male nuptial gift in P. napi clearly qualifies as both paternal investment and mating effort.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Baker HG, Baker I (1973) Amino acids in nectar and their evolutionary significance. Nature 241:543–545Google Scholar
  2. Boggs CL (1981a) Selection pressures affecting male nutrient investment at mating in Heliconiine butterflies. Evolution 35:931–940Google Scholar
  3. Boggs CL (1981b) Nutritional and life-history determinants of resource allocation in holometabolous insects. Am Nat 117:692–709Google Scholar
  4. Boggs CL (1990) A general model of the role of male-donated nutrients in female insect's reproduction. Am Nat 136:598–617Google Scholar
  5. Boggs CL, Gilbert LE (1979) Male contribution to egg production in butterflies evidence for transfer of nutrients at mating. Science 206:83–84Google Scholar
  6. Boggs CL, Watt WB (1981) Population structure of pierid butterflies. IV. Genetic and physiological investment in offspring by male Colias. Occologica 50:320–324Google Scholar
  7. Boggs CL, Smiley JT, Gilbert LE (1981) Patterns of pollen exploitation by Heliconius butterflies. Oecologia 48:284–289Google Scholar
  8. Bowen BJ, Codd CG, Gwynne DT (1984) The katydid spermatophore (Orthoptera: Tettigoniidae): Male nutritional investment and its fate in the mated female. Aust J Zool. 32:23–31Google Scholar
  9. Burns JM (1968) Mating frequency in natural populations of skippers and butterflies as determined by spermatophore counts. Proc Natl Acad Sci USA 61:852–859Google Scholar
  10. Chen PS (1984) The functional morphology and biochemistry of insect male accessory glands and their secretions. Annu Rev Entomol 29:233–255Google Scholar
  11. 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, New York, pp 291–370Google Scholar
  12. Ehrlich AH, Ehrlich PH (1978) Reproductive strategies in the butterflies: I. Mating frequency, plugging, and egg number. J Kansas Entomol Soc 51:666–697Google Scholar
  13. Forsberg J, Wiklund C (1989) Mating in the afternoon: time saving in courtship and remating by females of a polyandrous butterfly, Pieris napi. Behav Ecol Sociobiol 25:349–356Google Scholar
  14. Gilbert LE (1972) Pollen feeding and reproductive biology of Heliconius butterflies. Proc Natl Acad Sci USA 69:1403–1407Google Scholar
  15. Gromko MH, Gilbert DG, Richmond RC (1984) Sperm transfer and use in the multiple mating system of Drosophila. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, New York, pp 371–426Google Scholar
  16. Gwynne DT (1984) Courtship feeding increased female reproductive success in bush crickets. Nature 307:361–363Google Scholar
  17. Gwynne DT (1986) Stepfathers in insects and their pseudo-paternal investment. Ethology 71:74–77Google Scholar
  18. Gwynne DT (1988) Courtship feeding benefits the mating male's offspring. Behav Ecol Sociobiol 23:373–377Google Scholar
  19. Herman WS, Barker JF (1977) Effect of mating on monarch butterfly oogenesis. Experentia 33:688–689Google Scholar
  20. Jones KN, Odendaal FJ, Ehrlich PR (1986) Evidence against the spermatophore as paternal investmant in the checkerspot butterflies (Euphydryas: Nymphalidae) Am Midl Nat 116:1–6Google Scholar
  21. Labine P (1964) Population biology of the butterfly, Euphydryas editha. I. Barriers to multiple inseminations. Evolution 18:335–336Google Scholar
  22. Labine P (1966) The population biology of the butterfly, Euphydryas editha. IV. Sperm precedence — a preliminary report. Evolution 20:580–586Google Scholar
  23. Markow TA (1988) Drosophila males provide a material contribution to offspring sired by other males. Funct Ecol 2:77–79Google Scholar
  24. Markow TA, Gallagher PD, Krebs RA (1990) Ejaculate-derived nutritional contribution and female reproductive success in Drosophila mojavensis. Funct Ecol 4:67–73Google Scholar
  25. Obara Y (1982) Mate refusal hormone in the cabbage white butterfly? Naturwissenschaften 69:551–552Google Scholar
  26. Obara Y, Tateda H, Kuwabara M (1975) Mating behaviour of the cabbage white butterfly, Pieris rapae crucivora. V. Copulatory stimuli inducing changes of female response patterns. Zool Mag 84:71–76Google Scholar
  27. Oberhauser K (1988) Male monarch butterfly spermatophore mass and mating strategies. Anim Behav 36:1384–1388Google Scholar
  28. Oberhauser K (1989) Effects of spermatophores on male and female monarch butterfly reproductive success. Behav Ecol Sociobiol 25:237–246Google Scholar
  29. Oberhauser K (1992) Rate of ejaculate breakdown and intermating intervals in monarch butterflies. Behav Ecol Sociobiol 31:367–373Google Scholar
  30. Parker G, Simmons L (1989) Nuptial feeding in insects: Theoretical models of male and female interests. Ethology 82:3–26Google Scholar
  31. Pitnick S, Markow TA, Riedy MF (1991) Transfer of ejaculate and incorporation of male-derived substances by females in the nannoptera species group (Diptera: Drosophilidae). Evolution 45:774–780Google Scholar
  32. Rothschild M (1978) Hell's angels. Antenna 2:38–39Google Scholar
  33. Rutowski RL, Gilchrist GW (1986) Copulation in Colias eurytheme (Lepidoptera: Pieridae): patterns and frequency. J Zool 209:115–124Google Scholar
  34. Rutowski RL, Gilchrist GW, Terkanian B (1987) Female butterflies mated with recently mated males show reduced reproductive output. Behav Ecol Sociobiol 20:319–322Google Scholar
  35. Simmons L (1988) The contribution of multiple mating and spermatophore consumption to the lifetime reproductive success of female field crickets (Gryllus bimaculatus). Ecol Entomol 13:57–69Google Scholar
  36. Simmons L, Parker G (1989) Nuptial feeding in insects: Mating effort versus paternal investment. Ethology 81:332–343Google Scholar
  37. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, New YorkGoogle Scholar
  38. Sugawara C (1979) Stretch reception in bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behaviour. J Comp Physiol 130:191–199Google Scholar
  39. Svärd L, Wiklund C (1986) Different ejaculate delivey strategies in first versus subsequent matings in the swallowtail butterfly Papilio machaon. Behav Ecol Sociobiol 18:325–330Google Scholar
  40. Svärd L, Wiklund C (1998) Fecundity, egg weight and longevity in relation to multiple matings in the monarch butterfly. Behav Ecol Sociobiol 23:39–43Google Scholar
  41. Svärd L, Wiklund C (1989) Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav Ecol Sociobiol 24: 395–402Google Scholar
  42. Svärd L, Wiklund C (1991) The effect of ejaculate mass on female reproductive output in the European swallowtail butterfly Papilio machaon. J Insect Behavior 4:33–41Google Scholar
  43. Watanabe M (1988) Multiple matings increase the fecundity of the yellow swallowtail butterfly, Papilio xuthus, in summer generations. J Insect Behavior 1:17–30Google Scholar
  44. Watt WB, Hoch PC, Mills SG (1974) Nectar resource use by Colias butterflies. Chemical and visual aspects. Oecologia 14:353–374Google Scholar
  45. Wedell N, Arak A (1989) The wartbiter spermatophore and its effect on female reproductive output (Orthoptera: Tettigoniidae, Decticus verrucivorus). Behav Ecol Sociobiol 24:117–125Google Scholar
  46. Wedell N (1992) Protandry, spermatophore size and mate assessment in the wartbiter Decticus verucivorus (Orthoptera: Tettigoniidae). Behav Ecol Sociobiol 31:301–308Google Scholar
  47. Wickler W (1985) Stepfathers in insects and their pseudo-paternal investment. Z Tierpsychol 69:72–78Google Scholar
  48. Wickler W (1986) Mating costs versus paternal investment: a reply to Gwynne. Ethology 71:78–79Google Scholar
  49. Wiklund C, Forsberg J (1985) Courtship and mate discrimination between virgin and mated females in the orange tip butterfly, Anthocharis cardamines. Anim Behav 34:328–332Google Scholar
  50. Wiklund C, Forsberg J (1991) Sexual size dimorphism in relation to female polygamy and protandry in butterflies: a comparative study of Swedish Pieridae and Satyridae. Oikos 60:373–381Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Christer Wiklund
    • 1
  • Arja Kaitala
    • 1
  • Virpi Lindfors
    • 1
  • Johan Abenius
    • 1
  1. 1.Department of ZoologyUniversity of StockholmStockholmSweden

Personalised recommendations