The Behavioral Effects of a Carboxylesterase in Drosophila

  • Rollin C. Richmond
  • Suresh D. Mane
  • Laurie Tompkins


The analysis of the genetic bases of behavior and its adaptive significance is complex. Until recently, the genetic analysis of behavior relied largely on quantitative genetic methodology. While this approach has been successful in identifying the degree to which genetics influence the variability in behavioral traits, it has been unable to elucidate the mechanistic bases for adaptive behavior or to reveal the possible evolutionary histories of behavioral adaptations. Work in our laboratory has been concerned principally with an understanding of the evolutionary significance of polymorphisms at enzyme-coding loci in natural populations of Drosophila. Our work has concentrated on the function and adaptive significance of a carboxylesterase polymorphism—Esterase-6 (EST-6)—in Drosophila melanogaster Meigen (Richmond et al. 1980). This work has revealed that EST-6 has several effects on the reproductive biology of Drosophila. Among these effects is a direct influence on the sexual attractiveness of mated Drosophila females. This work reveals the complexity of interactions which a single locus, presumably coding for the structure of EST-6, can have on several aspects of reproductive behavior. Our findings further demonstrate the importance of a multi-disciplinary approach to problems of behavior genetics (Hirsch and McGuire 1982).


Virgin Female Seminal Fluid Female Reproductive Tract Sexual Attractiveness Sperm Transfer 
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Literature Cited

  1. Aceves-Pina, E. O. and W. G. Quinn. 1979. Learning in normal and mutant Drosophila larvae. Science 206: 93.PubMedCrossRefGoogle Scholar
  2. Aslund, S. E. and M. Rasmuson. 1976. Mating behavior as a fitness component in maintaining allozyme polymorphisms in Drosophila melanogaster. Hereditas 82: 175.PubMedCrossRefGoogle Scholar
  3. Averhoff, W. W. and R. H. Richardson. 1974. Pheromonal control of mating patterns in Drosophila melanogaster. Behav. Genet. 4: 207.PubMedCrossRefGoogle Scholar
  4. Averhoff, W. W. and R. H. Richardson. 1976. Multiple pheromone systems controlling mating in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 73: 591.PubMedCrossRefGoogle Scholar
  5. Boorman, E. and G. A. Parker. 1976. Sperm (ejaculate) competition in Drosophila melanogaster, and the reproductive value of females to males in relation to female age and mating status. Ecol. Entomol. 1: 145.CrossRefGoogle Scholar
  6. Brieger, G. and F. M. Butterworth. 1970. Drosophila melanogaster: Identity of male lipid in reproductive system. Science 167: 1262.PubMedCrossRefGoogle Scholar
  7. Butterworth, F. M. 1969. Lipids of Drosophila: A newly detected lipid in the male. Science 163: 1356.PubMedCrossRefGoogle Scholar
  8. Carson, H. L. 1981. Chromosomal tracing of evolution in a phylad of species related to Drosophila hawaiiensis. In W. R. Atchley and D. S. Woodruff, eds. Evolution and Speciation. Cambridge University Press, Cambridge.Google Scholar
  9. Davey, K. G. 1980. The physiology of reproduction in Rhodnius and other insects: Some questions. In M. Locke and D. S. Smith, eds. Academic Press, New York.Google Scholar
  10. Ehrman, L. 1966. Mating success and genotype frequency in Drosophila. Anim. Behav. 14: 332.PubMedCrossRefGoogle Scholar
  11. Ehrman, L. 1968. Frequency dependence of mating success in Drosophila pseudoobscura. Genet. Res. 11: 135.PubMedCrossRefGoogle Scholar
  12. Ehrman, L. and J. Probber. 1978. Rare Drosophila males: The mysterious matter of choice. Amer. Sci. 66: 216.Google Scholar
  13. Ehrman, L. and E. B. Spiess. 1969. Rare type mating advantage in Drosophila. Amer. Natur. 103: 675.CrossRefGoogle Scholar
  14. Gilbert, D. G. 1981. Ejaculate esterase 6 and initial sperm use by female Drosophila melanogaster. J. Insect Physiol. 27: 641.CrossRefGoogle Scholar
  15. Gilbert, D. G. and R. C. Richmond. 1982. Esterase 6 in Drosophila melanogaster: Reproductive function of active and null males at low temperature. Proc. Natl. Acad. Sci. USA. 79: 2962.PubMedCrossRefGoogle Scholar
  16. Gilbert, D. G., R. C. Richmond, and K. S. Sheehan. 1981. Studies of esterase 6 in Drosophila melanogaster. VII. The timing of remating in females inseminated by males having active or null alleles. Behav. Genet. 11: 195.PubMedCrossRefGoogle Scholar
  17. Gromko, D. G., and D. W. Pyle. 1978. Sperm competition, male fitness, and repeated mating by female Drosophila melanogaster. Evolution 32: 588.CrossRefGoogle Scholar
  18. Gromko, M. H., D. G. Gilbert, R. C. Richmond. 1984. Sperm transfer and use in the multiple mating system of Drosophila. In R. L. Smith, ed. Sperm Competition and the Evolution of Animal Mating Systems. Academic Press, New York.Google Scholar
  19. Heinstra, P. W. H. and G. E. Thorig. 1982. Multiple function of pteridines in Drosophila melahogaster. J. Insect. Physiol. 28: 847.CrossRefGoogle Scholar
  20. Hirsch, J. and T. R. McGuire. 1982. Behavior-Genetic Analysis. Hutchinson Ross Publishing Company, Stroudsburg, Pennsyslvania.Google Scholar
  21. Jallon, J-M, C. Antony, and T. Iwatsubo. 1981. Elements of chemical communication between Drosophilids and their modulation. Taniguchi Symposium on Biophysics, Kyoto.Google Scholar
  22. Kaneshiro, K. Y. 1980. Sexual isolation, speciation and the direction of evolution. Evolution 34: 437.CrossRefGoogle Scholar
  23. Kiefer, B. I. 1966. Ultrastructural abnormalities in developing sperm of X/O Drosophila melanogaster. Genetics 54: 1441.PubMedGoogle Scholar
  24. Langley, C. H., R. A. Voelker, A. J. Leigh-Brown, S. Ohnishi, B. Dickson, and E. Montgomery. 1981. Null allele frequencies at allozyme loci in natural populations of Drosophila melanogaster. Genetics 99: 151.PubMedGoogle Scholar
  25. Lefevre, G. and U. B. Jonsson. 1962. Sperm transfer, storage, displacement and utilization in Drosophila melanogaster. Genetics 47: 1719.PubMedGoogle Scholar
  26. Loher, W., I. Ganjian, I. Kubo, D. Stanley-Samuelson, and S. S. Tobe. 1981. Prostaglandins: Their role in egg-laying of the cricket Teleogryllus commodus. Proc. Natl. Acad. Sci. USA 78: 7835.PubMedCrossRefGoogle Scholar
  27. Mane, S., C. S. Tepper, and R. C. Richmond. 1983a. Studies of esterase 6 in Drosophila melanogaster. XIII. Purification and characterization of the two major isozymes. Biochem. Genet. 21:1019.PubMedCrossRefGoogle Scholar
  28. Mane, S., L. Tompkins, and R. C. Richmond. 1983b. A sex pheromone is synthesized in the reproductive tract of Drosophila melanogaster females by an enzyme and substrate provided by males. Science. 222:419.PubMedCrossRefGoogle Scholar
  29. Manning, A. 1962. A sperm factor affecting the receptivity of Drosophila melanogaster females. Nature 194: 252.CrossRefGoogle Scholar
  30. Manning, A. 1967. The control of sexual receptivity in female Drosophila. Anim. Behav. 15: 239.PubMedCrossRefGoogle Scholar
  31. Oakeshott, J. G., G. K. Chambers, J. B. Gibson, and D. A. Willcocks. 1981. Latitudinal relationships of esterase-6 and phophoglucomutase gene frequencies in Drosophila melanogaster. Heredity 47: 385.PubMedCrossRefGoogle Scholar
  32. Petit, C. 1958. Le determinisme genetique st psychopsysiologique de la competition sexuelle chez Drosophila melanogaster. Bull. Biol. Fr. Belg. 92:1.Google Scholar
  33. Pliske, T. E. and T. Eisner. 1969. Sex pheromone of the queen butterfly: biology. Science 164: 1170.PubMedCrossRefGoogle Scholar
  34. Prout, T. and J. Bundgaard. 1977. The population genetics of sperm displacement. Genetics 85: 95.PubMedGoogle Scholar
  35. Pruzan, A. 1976. Effects of age, rearing, and mating experiences on frequency dependent sexual selection in Drosophila melanogaster. Evolution 30: 130.CrossRefGoogle Scholar
  36. Pyle, D. W. and M. H. Gromko. 1978. Repeated mating by Drosophila melanogaster: The adaptive importance, Experientia. 34: 449.CrossRefGoogle Scholar
  37. Richmond, R. C. and A. S. Senior. 1981. Studies of esterase 6 in Drosophila melanogaster. IX. Kinetics of transfer to females, decay in females, and male recovery. J. Insect Physiol. 27: 849.CrossRefGoogle Scholar
  38. Richmond, R. C., D. G. Gilbert, K. B. Sheehan, M. H. Gromko, and F. M. Butterworth. 1980. Esterase 6 is involved in the reproduction of Drosophila melanogaster. Science 207: 1483.PubMedCrossRefGoogle Scholar
  39. Rodriques, V. 1980. Olfactory behavior of Drosophila melanogaster. In O. Siddiqi, P. Babu, L. Hall, and J. Hall, eds. Develoment and neurobiology of Drosophila. Plenum, New York.Google Scholar
  40. Rodriques, V. and O. Siddiqi. 1978. Genetic analysis of chemosensory pathway. Proc. Indian Acad. Sci. 87B: 147.Google Scholar
  41. Sheehan, K. B., R. C. Richmond, and B. J. Cochrane. 1979. Studies of esterase 6 in Drosophila melanogaster. III. The developmental pattern and tissue distribution. Insect Biochem. 9: 443.CrossRefGoogle Scholar
  42. Stanley-Samuelson, D. W. and W. Loher. 1983. Arachidonic and other long-chain polyun-saturated fatty acids in spermatophores and spermathecae of Teleogryllus commodus: Significance in prostaglandin-mediated reproductive behaviour. J. Insect. Physiol. 29:41.CrossRefGoogle Scholar
  43. Stein, S. P., C. S. Tepper, N. D. Able and R. C. Richmond. 1984. Studies of esterase 6 in Drosophila melanogaster. 2XVI. Synthesis occurs in the male reproductive tract (anterior ejaculatory duct) and is modulated by juvenile hormone. Insect Biochem. 14:527.CrossRefGoogle Scholar
  44. Tompkins, L., J. C. Hall, and L. M. Hall. 1980. Courtship-stimulating compounds from normal and mutant Drosophila. J. Insect Physiol. 26: 689.CrossRefGoogle Scholar
  45. Tompkins, L. and J. C. Hall. 1981. The different effects on courtship of volatile compounds from mated and virgin Drosophila females. J. Insect Physiol. 27: 17.CrossRefGoogle Scholar
  46. Tompkins, L., A. C. Gross, J. C. Hall, D. A. Gailey, and R. W. Siegel. 1982. The role of female movement in the sexual behavior of Drosophila melanogaster. Behav. Genetics 12: 295.CrossRefGoogle Scholar
  47. Voelker, R. A., C. H. Langley, A. J. Leigh-Brown, S. Ohnishi, B. Dickson, E. Montgomery, and S. C. Smith. 1980. Enzyme null alleles in natural populations of Drosophila melanogaster. Frequencies in a North Carolina population. Proc. Natl. Acad. Sci. USA 77: 1091.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1986

Authors and Affiliations

  • Rollin C. Richmond
    • 1
  • Suresh D. Mane
    • 1
  • Laurie Tompkins
    • 2
  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA
  2. 2.Department of BiologyTemple UniversityPhiladelphiaUSA

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