Sperm transfer and storage in relation to sperm competition in Callosobruchus maculatus

Abstract

This paper examines the underlying mechanisms of sperm competition in the beetle Callosobruchus maculatus (F.) (Coleoptera: Bruchidae). Recently developed mathematical models of sperm competition are combined with an empirical investigation of the processes of sperm transfer and storage. During a single insemination virgin males transfer approximately 46000 sperm, 85% more sperm than females can effectively store in their spermathecae. Many of these sperm remain in the bursa copulatrix where they are apparently rapidly degraded and can therefore play no role in fertilization. The spermatheca (primary site of sperm storage) is filled by a single insemination and sperm are lost from this organ at a constant rate. This rate of sperm loss from the spermatheca is insufficient for sperm mixing (without displacement) or sperm stratification to account for the degree of last male sperm precedence measured as P 2; the proportion of offspring fathered by the second male to mate reported for this species (P 2 = 0.83, when two inseminations are separated by 24 h). Models of sperm displacement correctly predict high levels of sperm precedence although the precision of these predictions is limited because the proportion of sperm entering the spermatheca cannot be accurately determined. The results suggested that last male sperm precedence in C. maculatus the result of sperm displacement, although the exact mechanism of displacement (sperm-for-sperm or fluid displacement) remains unknown. Possible constraints imposed by female genital anatomy on sperm displacement are discussed.

This is a preview of subscription content, log in to check access.

References

  1. Baker RR, Bellis MA (1988) “Kamikaze” sperm in mammals? Anim Behav 36:936–939

    Google Scholar 

  2. Baker RR, Bellis MA (1989) Elaboration of the kamikaze sperm hypothesis: a reply to Harcourt. Anim Behav 37:865–867

    Google Scholar 

  3. Bawa SR, Kanwar KC (1975) The structure of Callosobruchus maculatus spermatozoon. J Submicrosc Cytol 7:71–79

    Google Scholar 

  4. Bedford JM (1970) The saga of mammalian sperm from ejaculation to syngamy. In: Gibian H., Plotz E.J. (eds) Mammalian reproduction. Springer, Berlin Heidelberg New York, pp 124–182

    Google Scholar 

  5. Birkhead TR (1991) Sperm depletion in the Bengalese finch Lonchura striata. Behav Ecol 2:267–275

    Google Scholar 

  6. Birkhead TR, Møller AP, Sutherland WJ (1993) Why do females make it so difficult for males to fertilize their eggs? J Theor Biol 161:51–60

    Google Scholar 

  7. Brillard JP, Bakst MR (1990) Quantification of spermatozoa in the sperm-storage tubules of turkey hens and its relation to sperm numbers in the perivitelline layer of eggs. Biol Reprod 43:271–275

    Google Scholar 

  8. Cohen J (1973) Crossovers, sperm redundancy and their close association. Heredity 31:408–413

    Google Scholar 

  9. Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610

    Google Scholar 

  10. Eady PE (1991) Sperm competition in Callosobruchus maculatus (Coleoptera: Bruchidae): a comparison of two methods used to estimate paternity. Ecol Entomol 16:45–53

    Google Scholar 

  11. Eady PE (1992) Sperm competition in Callosobruchus maculatus. PhD Thesis, University of Sheffield, Sheffield, UK

    Google Scholar 

  12. Eady PE (1994) Intraspecific variation in sperm precedence in Callosobruchus maculatus. Ecol Entomol 19:11–16

    Google Scholar 

  13. Fox CW (1993) Multiple mating, lifetime fecundity and female mortality of the bruchid beetle Callosobruchus maculatus (Coleoptera: Bruchidae). Funct Ecol 7:203–208

    Google Scholar 

  14. Gwynne DT (1984) Male mating effort, confidence of paternity and insect sperm competition. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic Press, London, pp 117–149

    Google Scholar 

  15. Harcourt AH (1989) Deformed sperm are probably not adaptive. Anim Behav 37:863–865

    Google Scholar 

  16. Harcourt AH (1991) Sperm competition and the evolution of non-fertilizing sperm in mammals. Evolution 45:314–328

    Google Scholar 

  17. Lamb JF, Ingram CG, Johnson RM (1980) Essentials of physiology. Blackwell, Oxford

    Google Scholar 

  18. Lessells CM, Birkhead TR (1990) Mechanisms of sperm competition in birds: mathematical models. Behav Ecol Sociobiol 27:325–337

    Google Scholar 

  19. Nakatsuru K, Kramer DL (1982) Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces: Characidae). Science 216:753–755

    Google Scholar 

  20. Ouedraogo AP (1978) Étude de quelques aspects de la biologic de Callosobruchus maculatus F (Coléoptère: Bruchidae) et de l'influence des facteurs externes stimulants (plante hôte et copulation) sur l'activité reproductrice de la femelle. Thése 3eme Cycle, University Paul Sabatier, Toulouse, France

    Google Scholar 

  21. Parker GA, Simmons LW (1991) A model of constant random sperm displacement during mating: evidence from Scatophaga. Proc R Soc Lond B 249:107–115

    Google Scholar 

  22. Parker GA, Simmons LW, Kirk H (1990) Analysing sperm competition data: simple models for predicting mechanisms. Behav Ecol Sociobiol 27:55–65

    Google Scholar 

  23. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, San Francisco

    Google Scholar 

  24. Villavaso EJ (1975) Functions of the spermathecal muscle of the boll weevil, Anthonomus grandis. J Insect Physiol 21:1275–1278

    Google Scholar 

  25. Wickler W (1985) Stepfathers in insects and their pseudo-parental investment. Z Tierpsychol 69:72–78

    Google Scholar 

  26. Wilson K, Hill L (1989) Factors affecting egg maturation in the bean weevil Callosobruchus maculatus. Physiol Entomol 14:115–126

    Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Eady, P. Sperm transfer and storage in relation to sperm competition in Callosobruchus maculatus . Behav Ecol Sociobiol 35, 123–129 (1994). https://doi.org/10.1007/BF00171502

Download citation

Key words

  • Bruchidae
  • Sperm competition
  • Sperm storage