Behavior Genetics

, Volume 14, Issue 5, pp 441–478

A few chemical words exchanged byDrosophila during courtship and mating

  • Jean-Marc Jallon


Experimental evidence and speculation relative to chemical messages exchanged byDrosophila during courtship and mating are reviewed. Only the speciesD. melanogaster andD. simulans are considered in detail.

Emphasis is put on female aphrodisiacs, as they clearly participate in sex and species recognition. All the aphrodisiac molecules described are unsaturated long-chain hydrocarbons, and position 7 for a double bond seems important in both species. InD. melanogaster, only females are able to make 7,11-dienes, compounds which stimulate males of this species to court. InD. simulans, 7-tricosene plays a similar role but is produced by both sexes as well as maleD. melanogaster. In both species, polymorphism is shown for these molecules. Their biosynthesis is also considered and both preliminary biochemical and genetic data are introduced.

Male-specific compounds which regulate male and female behaviors are also reviewed. For example,cis-vaccenyl acetate inhibits male courtship; one or two peptides control the female's receptivity and egg laying. Such compounds are transferred from males to females together with sperm.

Key Words

Drosophila courtship pheromones 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adams, T. S., Dillwith, J. W., and Blomquist, G. J. (1984). The role of 20-hydroxyecdysone in house fly sex pheromone synthesis.J. Insect Physiol. 30:287–294.Google Scholar
  2. Antony, C. (1980).Etude du système phéromonal de Drosophila melanogaster, Thèse de Specialité, Université de Paris VI, Paris.Google Scholar
  3. Antony, C., and Jallon, J.-M. (1980). Evolution des hydrocarbures comportementalement actifs deDrosophila melanogaster au cours de la maturation sexuelle.C.R. Acad. Sci. Paris 252:239–242.Google Scholar
  4. Antony, C., and Jallon, J.-M. (1982). The chemical basis for sex recognition inJ. Insect Physiol. 28:873–880.Google Scholar
  5. Arpino, P., Van Dorrselaer, A., Sevier, K., and Ourisson, G. (1972). Cires aeriennes dans une foret de pins.C.R. Acad. Sci. Paris 275:2837–2840.Google Scholar
  6. Audit-Lamour, C., and Busson, D. (1981). Oegenesis defects in the ecd1 mutant ofDrosophila melanogaster, deficient in ecdysteroid at high temperature.J. Ins. Physiol. 27:829–837.Google Scholar
  7. Averhoff, W., and Richardson, R. (1974). Pheromone control of mating patterns inDrosophila melanogaster.Behav. Genet. 4:207–225.PubMedGoogle Scholar
  8. Averhoff, W., and Richardson, R. (1976). Multiple pheromone system controlling mating inDrosophila melanogaster.Proc. Natl. Acad. Sci. USA 73:591–593.PubMedGoogle Scholar
  9. Bastock, M., and Manning, A. (1955). The courtship ofDrosophila melanogaster.Behaviour 8:85–111.Google Scholar
  10. Baumann, H. (1974). The isolation, partial characterization and biosynthesis of the paragonial substances, PS-1 and PS-2, ofDrosophila funebris.J. Insect Physiol. 20:2181–2194.PubMedGoogle Scholar
  11. Baumann, H. (1975). Biological effects of paragonial substances PS-1 and PS-2 in females ofDrosophila funebris.J. Insect. Physiol. 20:2347–2362.Google Scholar
  12. Begg, M. K., and Hogben, L. (1946).Proc. R. Soc. Lond. B 133:1–19.Google Scholar
  13. Benamar, O. (1982).Caracterisation et étude génétique de la production d'un composé aphrodisiaque de l'espèce Drosophila simulans, Thèse de Spécialité, Université de Paris VI, Paris.Google Scholar
  14. Bennet-Clark, M., and Ewing, A. (1969). Pulse interval as a critical parameter in the courtship song ofDrosophila melanogaster.Anim. Behav. 17:755–759.Google Scholar
  15. Benzer, S. (1973). Genetic dissection of behavior.Sci. Am. 229:24–37.PubMedGoogle Scholar
  16. Blomquist, G., and Jackson, L. (1979). Chemistry and biochemistry of insect waxes.Prog. Lipid Res. 17:319–345.PubMedGoogle Scholar
  17. Brown, R. C. G. (1966). Courtship behavior in theDrosophila obscura group. I. D. Pseudoobscura.Behaviour 23:61–106.Google Scholar
  18. Burnet, B., and Connolly, K. (1981). Gene action and the analysis of behavior.Br. Med. Bull. 37:107–113.PubMedGoogle Scholar
  19. Burnet, B., Connolly, K., and Dennis, L. (1971). The function and processing of auditory information in the courtship behavior ofD. melanogaster.Anim. Behav. 19:409–415.PubMedGoogle Scholar
  20. Butterworth, F. M. (1969). Lipids ofDrosophila: A newly detected lipid in the male.Science 163:1356–1357.PubMedGoogle Scholar
  21. Carlson, D., Mayer, M., Silhacek, D., James, J., Beroza, M., and Bierl, B. (1971). Sex attractant pheromone of the house fly: Isolation, identification and synthesis.Science 174:76–77.PubMedGoogle Scholar
  22. Chen, P. S., and Bühler, R. (1970). Paragonial substance and other free ninhidrin-positive components in male and female adults ofDrosophila melanogaster.J. Insect Physiol. 16:615–627.PubMedGoogle Scholar
  23. Chen, P. S., and Diem, C. (1961). A sex-specific minhydrin-positive substance found in the paragonia of adult males ofDrosophila melanogaster.J. Insect Physiol. 7:289–298.Google Scholar
  24. Connolly, K., and Cook, K. (1973). Rejection responses by femaleDrosophila melanogaster: Their ontogeny, causality and effects upon behaviour of the courting males.Behaviour 44:122–146.Google Scholar
  25. Cook, R. (1978). The reproductive behavior of gynandromorphicDrosophila melanogaster.Z. Naturforsch. 33c:744–754.Google Scholar
  26. Cook, R., and Cook, A. (1975). The attractiveness to males of femaleDrosophila melanogaster: Effects of mating, age and diet.Anim. Behav. 23:521–526.PubMedGoogle Scholar
  27. Cowling, D. E., and Burnet, B. (1981). Courtship songs and genetic control of their acoustic characteristics in sibling species of theDrosophila melanogaster subgroup.Anim. Behav. 29:924–935.Google Scholar
  28. Dethier, V. G. (1971).The Physiology of Insect Senses, Chapman and Hall, London.Google Scholar
  29. Dillwith, J. W., and Blomquist, G. J. (1982). Site of sex pheromone biosynthesis in the female housefly,Musca domestica.Experientia 38:471–473.Google Scholar
  30. Dillwith, J. W., Blomquist, G. J., and Nelson, D. R. (1981). Biosynthesis of the hydrocarbons components of the sex pheromone of the housefly,Musca domestica.Insect. Biochim. 11:187–197.Google Scholar
  31. Diehl, P. A. (1975). Synthesis and release of hydrocarbons by the oenocytes of the desert locust.J. Insect Physiol. 21:1237–1246.Google Scholar
  32. Dumpert, K. (1978). Spider odor receptor: Electrophysiological proof.Experientia 34:754–755.Google Scholar
  33. Ehrman, L. (1972). A factor influencing the rare male mating advantage.Behav. Genet. 2:69–78.PubMedGoogle Scholar
  34. Ehrman, L. (1978). Sexual behavior. In Ashburner, M., and Wright, T. R. F. (eds.),The Genetics and Biology of Drosophila,Vol. 2b, Academic Press, London, pp. 127–180.Google Scholar
  35. Ewing, A. (1983). Functional aspects of Drosophila courtship.Biol. Rev. 58:275–292.Google Scholar
  36. Ewing, A., and Manning, A. (1963). The effect of exogenous scent on the mating ofDrosophila melanogaster.Anim. Behav. 27:343–349.Google Scholar
  37. Fish, B. R. (1972).Science 175:1239.PubMedGoogle Scholar
  38. Fox, A. S. (1956). Chromatographic differences between males and females inDrosophila melanogaster and role of X and Y chromosomes.Physiol. Zool. 29:288–298.Google Scholar
  39. Fuchs, M. S., and Hiss, E. A. (1970). The partial purification of the protein components of matrone fromAedes aegypti.J. Insect Physiol. 16:931–939.PubMedGoogle Scholar
  40. Fuyama, Y. (1983). Species-specificity of paragonial substances as an isolating mechanism.Experientia 39:190–192.Google Scholar
  41. Garcia-Bellido, A. (1964). Das sekrit der paragonien als stimulus der fekunditat bei weibchen vonDrosophila melanogaster.Z. Naturforsch. 19b:491–495.Google Scholar
  42. Garen, A., Kauvar, L., and Lepesant, J. A. (1977). Roles of ecdysone inDrosophila development.Proc. Natl. Acad. Sci. USA 74:5099–5103.Google Scholar
  43. Grossfield, J. (1966). The influence of light on the mating behavior ofDrosophila.Univ. Tex. Publ. 6615:147–176.Google Scholar
  44. Grossfield, J. (1971). Geographic distribution and light-dependent behavior inDrosophila.Proc. Natl. Acad. Sci. 68:2669–2673.PubMedGoogle Scholar
  45. Hagedorn, H. H. (1981). In Clark, W. H., and Adams, T. S. (eds.)Ecdysone, a Gonadal Hormone in Insects, Elsevier North-Holland, Amsterdam, pp. 97–107.Google Scholar
  46. Hall, J. C. (1978a). Behavioral analysis inDrosophila mosaics. In Gehring, W. J. (ed.),Genetics Mosaics and Cell Differentiation, Springer-Verlag, Berlin, pp. 259–305.Google Scholar
  47. Hall, J. C. (1978b). Courtship among males due to male-sterile mutation inDrosophila melanogaster.Behav. Genet. 8:125–141.PubMedGoogle Scholar
  48. Hall, J. C. (1982). Genetics of the nervous system inDrosophila.Q. Rev. Biophys. 15:1–223.PubMedGoogle Scholar
  49. Hedin, P. A. Niemeyer, C. S., Gueldner, R. C., and Thompson, A. C. (1972). A gas chromatographic survey of the volatile fractions of twenty species of insects from eight orders.J. Insect Physiol. 18:555–564.Google Scholar
  50. Hildreth, P. E. (1965). Doublesex, a recessive gene that transforms both males and females ofDrosophila into intersexes.Genetics 51:659–678.PubMedGoogle Scholar
  51. Hodgkin, N. M., and Bryant, P. (1978). Scanning electron microscopy of the adult ofDrosophila melanogaster. In Ashburner, M., and Wright, T. R. F. (eds.),The Genetics and Biology of Drosophila, Academic Press, London, pp. 337–358.Google Scholar
  52. Hodosh, R. J., Klough, E. M., and Ringo, J. M. (1979). The morphology of the sex pheromone gland inDrosophila grimshawii.J. Morphol. 161:177–184.Google Scholar
  53. Howard, R. W., and Blomquist, G. J. (1982). Chemical ecology and biochemistry of insect hydrocarbons.Annu. Rev. Entomol. 27:149–172.Google Scholar
  54. Ismail, M. T. (1984).Mise en évidence d'une phéromone sexuelle volatile chez les femelles de Culicoides nubeculoses.Etude des facteurs ethologiques et physiologiques de son emission. Approches histologiques et biochimiques de sa production, Thèse de Doctorat d'Etat, Université de Strasbourg, Strasbourg.Google Scholar
  55. Jackson, L., Arnold, M., and Blomquist, G. (1981). Surface lipids ofD. melanogaster: Comparison between wild types and yellow mutants.Insect Biochem. 11:87–91.Google Scholar
  56. Jallon, J.-M., and Hotta, Y. (1979). Genetic and behavioral studies of female sex-appeal inDrosophila.Behav. Genet. 8:487–502.Google Scholar
  57. Jallon, J.-M., and Hotta, Y. (1980). A proposal for sex-appealless mutant hunting.Dros. Inform. Serv. 55:65.Google Scholar
  58. Jallon, J.-M., and Hotta, Y. (1981). Nonchemical messages of the femaleDrosophila melanogaster. In Hotta, Y. (ed.),Taniguchi Symposia in Biophysics No. 7, University of Tokyo, Tokyo, pp. 136–144.Google Scholar
  59. Jallon, J.-M., Antony, C., Gallois, M., and Venard, R. (1980). Première caractérisation de substances aphrodisiaques chezDrosophila melanogaster.C.R. Acad. Sci. 292:1147–1149.Google Scholar
  60. Jallon, J.-M., Antony, C., and Benamar, O. (1981a). Un anti-aphrodisiac produit par les mâles deDrosophila melanogaster et transferé aux femelles lors de la copulation.C.R. Acad. Sci. Paris 292:1147–1149.Google Scholar
  61. Jallon, J.-M., Antony, C., and Iwatsubo, T. (1981b). Elements of chemical communication between Drosophilids and their modulation. In Hotta, Y. (ed.).Taniguchi Symposia in Biophysics No. 7, University of Tokyo, Tokyo, pp. 105–135.Google Scholar
  62. Jallon, J.-M., Benamar, O., Luyten, I., and Antony C. (1982). Modulations de la production des hydrocarbures cuticulaires aphrodisiaques des Drosophilides résultant de perturbation génétiques et physiologiques. In Descoins, C. (ed.),Colloques de l'INRA No. 7.Google Scholar
  63. Jeffcoat, R. (1979). The biosynthesis of unsaturated fatty acids and its control in mammalian liver.Essays Biochem. 15:1–36.PubMedGoogle Scholar
  64. Katase, H., and Chino, H. (1982). Transport of hydrocarbons by the lipophorin of insect hemolymph.Biochim. Biophys. Acta 710:341–348.Google Scholar
  65. Kyriacou, C. P., and Hall, J. C. (1980). Circadian rhythm mutations inDrosophila melanogaster affect short-term fluctuations in the male's courtship song.Proc. Natl. Acad. Sci. USA 77:6729–6733.PubMedGoogle Scholar
  66. Langley, P., and Carlson, D. (1983). Biosynthesis of contact sex pheromone in the female tsetse fly;Glossina morsitans morsitans.J. Insect Physiol. 29:825–831.Google Scholar
  67. Leahy, M. G. (1966). Egg deposition inD. melanogaster increased by transplant of male paragonia.Dros. Inform. Serv. 41:45.Google Scholar
  68. Leopold, R. (1976). The role of male accessory glands in insect reproduction.Annu. Rev. Entomol. 199–221.Google Scholar
  69. Luyten, I. (1982). Variations intraspécifiques et interspécifiques des hydrocarbures cuticulaires chezDrosophila simulans C.R. Acad. Sci. Paris 295:723–736.Google Scholar
  70. Luyten, I. (1983).Variations intra- et interspécifiques des hydrocarbures cuticulaires et des interactions comportementales chez quatre espèces affines du sous-groupe melanogaster, Thèse de Spécialité, Université de Paris VII, Paris.Google Scholar
  71. McRobert, S., and Tompkins, L. (1983). Courtship of young males is ubiquitous inDrosophila melanogaster.Behav. Genet. 13:517–523.PubMedGoogle Scholar
  72. Mane, S. D., Tompkins, L., and Richmond, R. C. (1983). Male esterase 6 catalyzes the synthesis of a sex pheromone inDrosophila melanogaster femalesScience 222:419–421.Google Scholar
  73. Manning, A. (1959a). The sexual behaviour of two siblingDrosophila species.Behaviour 15:123–145.Google Scholar
  74. Manning, A. (1959b). The sexual isolation betweenD. melanogaster andD. simulans.Anim. Behav. 7:60–65.Google Scholar
  75. Manning, A. (1967). The control of sexual receptivity in femaleDrosophila melanogaster.Anim. Behav. 15:239–250.PubMedGoogle Scholar
  76. Merle, J. (1968). Fonctionnement ovarien et réceptivité sexuelle deDrosophila melanogaster après implantation de fragments de l'appareil genital mâle.J. Insect Physiol. 14:1159–1168.PubMedGoogle Scholar
  77. Merrell, D. J. (1949). Selective mating inDrosophila melanogaster.Genetics 34:370–389.Google Scholar
  78. Miller, A. (1950). The internal anatomy and histology of the imago ofDrosophila melanogaster. In Demerec, M. (ed.),Biology of Drosophila, John Wiley and Sons, New York, pp. 420–536.Google Scholar
  79. Nelson, D. R., Adams, T. S., and Pomonis, J. G. (1969). Initial studies on the extraction of the active substance inducing monocoitic behavior inMusca domestica, Phormia regina and Cochliomya hominovorar.J. Econ. Entomol. 62:634–639.Google Scholar
  80. Nissani, N. (1977). Gynandromorph analysis of some aspects of sexual behavior ofDrosophila melanogaster.Anim. Behav. 5:351–366.Google Scholar
  81. Orssaud, L., and Laugé, G. (1982). Etude histologique de l'appareil génital du mutant d'intersexualite double deDrosophila melanogaster.Int. J. Insect Morphol. Embryol. 11:53–67.Google Scholar
  82. Pechine, J.-M., Perez, F., Antony, C., and Jallon, J.-M. (1984). A further characterization ofDrosophila cuticular hydrocarbons using a simple method to localize double bonds (submitted for publication).Google Scholar
  83. Postlewaith, J. M., and Handler, A. (1978). Nonvitellogenic female sterile mutants and the regulation of vitellogenesis inDrosophila melanogaster.Dev. Biol. 67:202–213.PubMedGoogle Scholar
  84. Richmond, R., Gilbert, D., Sheehan, K., Gromko, M., and Butterworth, F. (1980). Esterase 6 and reproduction inDrosophila melanogaster.Sciences 207:1483–1485.Google Scholar
  85. Robertson, H. M. (1983). Chemical stimuli eliciting courtship by males inD. melanogaster.Experientia 39:333–335.Google Scholar
  86. Rodrigues, V., and Siddiqi, O. (1978). Genetic analysis of chemosensory pathway.Proc. Ind. Acad. Sci. 87B;147–160.Google Scholar
  87. Santoso, T. (1983).Approche de la variabilité des hydrocarbures cuticulaires des Drosophiles et de leur contrôle génétique, Diplôme d'Etudes Approfondies, Université de Paris VI, Paris.Google Scholar
  88. Schlein, Y., Galun, R., and Ben-Eliahu, M. N. (1981). Receptors of sex pheromones and abstinons inMusca domestica andGlossina morsitans.J. Chem. Ecol. 7:291–301.Google Scholar
  89. Shorey, H. H. (1976).Animal communication by pheromones Academic Press, New York.Google Scholar
  90. Shorey, H., and Bartell, R. (1970). Role of a volatile sex pheromone in stimulating male courtship behaviour inDrosophila melanogaster.Anim. Behav. 18:159–164.PubMedGoogle Scholar
  91. Siegel, R. G., and Hall, J. C. (1979). Conditioned responses in courtship behavior of normal and mutantDrosophila.Proc. Natl. Acad. Sci. USA 76:3430–3434.Google Scholar
  92. Spence, G. E., Hoffmann, A. A., and Parsons, P. A. (1984). Habitat marking, males attracted to residual odours of twoDrosophila species.Experientia (in press).Google Scholar
  93. Spieth, H. (1974). Courtship behavior inDrosophila.Annu. Rev. Entomol. 19:385–405.PubMedGoogle Scholar
  94. Spieth, H., and Hsu, T. (1950). The influence of light on the mating behavior of seven species of theDrosophila melanogaster species group.Evolution 4:316–325.Google Scholar
  95. Spieth, H. T., and Ringo, J. M. (1983). Mating and sexual isolation inDrosophila. In Ashburner, M., Carson, H., and Thompson, J. (eds.),The Genetics and Biology of Drosophila, Vol. 3c, Academic Press, London, pp. 224–284.Google Scholar
  96. Strambi, C., Strambi, A., de Reggi, M. L., Hirn M. H., and De Laage, M. A. (1981). Radioimmuno assay of insect juvenile hormones and of their diol derivatives.Eur. J. Biochem. 118:401–406.PubMedGoogle Scholar
  97. Sturtevant, A. (1915). Experiments on sex recognition and the problem of sexual selection inDrosophila.J. Anim. Behav. 5:351–366.Google Scholar
  98. Tompkins, L., and Hall, J. C. (1981a). The different effects on courtship of volatile compounds from mated and virginDrosophila females.J. Insect Physiol. 27:17–21.Google Scholar
  99. Tompkins, L., and Hall, J. C. (1981b).Drosophila males produce a pheromone which inhibits courtship.Z. Naturforsch. 36c:694–695.Google Scholar
  100. Tompkins, L., Hall, J. C., and Hall, L. (1980). Courtship stimulating volatile compounds from normal and mutantDrosophila.J. Insect Physiol. 26:689–697.Google Scholar
  101. Tompkins, L., Gross, A., Hall, J., Gailey, D., and Siegel, R. (1982). The role of female movement in the sexual behavior ofD. melanogaster.Behav. Genet. 12:295–307.PubMedGoogle Scholar
  102. Tompkins, L., Siegel, R., Gailey, D., and Hall, J., (1983). Conditioned courtship inDrosophila and its mediation by association of chemical cues.Behav. Genet. 13:565–578.PubMedGoogle Scholar
  103. van den Berg, M. J., Thomas, G., Hendriks, M., and Van Delden (1983) A reexamination of the negative assortative mating phenomenon and its underlying mechanism inDrosophila melanogaster.Behav. Genet. 14:45–61.Google Scholar
  104. Venard, R. (1980). Attractants in the courtship behavior ofDrosophila melanogaster. In Siddiqi, O., Babu, P., Hall, L. M., and Hall, J. C. (eds.),Development and Neurobiology of Drosophila, Plenum Press, New York, pp. 457–465.Google Scholar
  105. Venard, R., and Jallon, J.-M. (1980). Evidence for an aphrodisiac pheromone of femaleDrosophila.Experientia 36:211–212.Google Scholar
  106. Venard, R., and Pichon, Y. (1983). Electrophysiological analysis of the peripheral response to odours in wild type and smell-deficient olf C mutant ofDrosophila melanogaster.J. Insect Physiol. 30:1–5.Google Scholar
  107. von Schilcher, F. (1976). The role of auditory stimuli in the courtship ofDrosophila melanogaster.Anim. Behav. 24:18–26.Google Scholar
  108. Watanabe, T., Lee, W. H., Inoue, Y., and Kawanishi, M. (1977). Genetic variation of the hybrid crossability betweenD. melanogaster andD. simulans.Jap. J. Genet. 52:1–8.Google Scholar
  109. Wigglesworth, V. B. (1974).Insect Physiology, Chapman and Hall, London.Google Scholar
  110. Wood, D., and Ringo, J. (1980). Male mating discrimination inD. melanogaster, D. simulans and their hybrids.Evolution 34:320–329.Google Scholar

Copyright information

© Plenum Publishing Corporation 1984

Authors and Affiliations

  • Jean-Marc Jallon
    • 1
  1. 1.Laboratoire d'Enzymologie PhysicochimiqueCentre de Génétique Moléculaire duCNRSGif-sur-YvetteFrance

Personalised recommendations