Skip to main content
Log in

A few chemical words exchanged byDrosophila during courtship and mating

  • Published:
Behavior Genetics Aims and scope Submit manuscript

Summary

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 

  • Antony, C. (1980).Etude du système phéromonal de Drosophila melanogaster, Thèse de Specialité, Université de Paris VI, Paris.

    Google Scholar 

  • 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 

  • Antony, C., and Jallon, J.-M. (1982). The chemical basis for sex recognition inJ. Insect Physiol. 28:873–880.

    Google Scholar 

  • 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 

  • 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 

  • Averhoff, W., and Richardson, R. (1974). Pheromone control of mating patterns inDrosophila melanogaster.Behav. Genet. 4:207–225.

    PubMed  Google Scholar 

  • Averhoff, W., and Richardson, R. (1976). Multiple pheromone system controlling mating inDrosophila melanogaster.Proc. Natl. Acad. Sci. USA 73:591–593.

    PubMed  Google Scholar 

  • Bastock, M., and Manning, A. (1955). The courtship ofDrosophila melanogaster.Behaviour 8:85–111.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • Begg, M. K., and Hogben, L. (1946).Proc. R. Soc. Lond. B 133:1–19.

    Google Scholar 

  • 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 

  • 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 

  • Benzer, S. (1973). Genetic dissection of behavior.Sci. Am. 229:24–37.

    PubMed  Google Scholar 

  • Blomquist, G., and Jackson, L. (1979). Chemistry and biochemistry of insect waxes.Prog. Lipid Res. 17:319–345.

    PubMed  Google Scholar 

  • Brown, R. C. G. (1966). Courtship behavior in theDrosophila obscura group. I. D. Pseudoobscura.Behaviour 23:61–106.

    Google Scholar 

  • Burnet, B., and Connolly, K. (1981). Gene action and the analysis of behavior.Br. Med. Bull. 37:107–113.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Butterworth, F. M. (1969). Lipids ofDrosophila: A newly detected lipid in the male.Science 163:1356–1357.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • Cook, R. (1978). The reproductive behavior of gynandromorphicDrosophila melanogaster.Z. Naturforsch. 33c:744–754.

    Google Scholar 

  • Cook, R., and Cook, A. (1975). The attractiveness to males of femaleDrosophila melanogaster: Effects of mating, age and diet.Anim. Behav. 23:521–526.

    PubMed  Google Scholar 

  • 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 

  • Dethier, V. G. (1971).The Physiology of Insect Senses, Chapman and Hall, London.

    Google Scholar 

  • 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 

  • 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 

  • Diehl, P. A. (1975). Synthesis and release of hydrocarbons by the oenocytes of the desert locust.J. Insect Physiol. 21:1237–1246.

    Google Scholar 

  • Dumpert, K. (1978). Spider odor receptor: Electrophysiological proof.Experientia 34:754–755.

    Google Scholar 

  • Ehrman, L. (1972). A factor influencing the rare male mating advantage.Behav. Genet. 2:69–78.

    PubMed  Google Scholar 

  • 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 

  • Ewing, A. (1983). Functional aspects of Drosophila courtship.Biol. Rev. 58:275–292.

    Google Scholar 

  • Ewing, A., and Manning, A. (1963). The effect of exogenous scent on the mating ofDrosophila melanogaster.Anim. Behav. 27:343–349.

    Google Scholar 

  • Fish, B. R. (1972).Science 175:1239.

    PubMed  Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Fuyama, Y. (1983). Species-specificity of paragonial substances as an isolating mechanism.Experientia 39:190–192.

    Google Scholar 

  • Garcia-Bellido, A. (1964). Das sekrit der paragonien als stimulus der fekunditat bei weibchen vonDrosophila melanogaster.Z. Naturforsch. 19b:491–495.

    Google Scholar 

  • Garen, A., Kauvar, L., and Lepesant, J. A. (1977). Roles of ecdysone inDrosophila development.Proc. Natl. Acad. Sci. USA 74:5099–5103.

    Google Scholar 

  • Grossfield, J. (1966). The influence of light on the mating behavior ofDrosophila.Univ. Tex. Publ. 6615:147–176.

    Google Scholar 

  • Grossfield, J. (1971). Geographic distribution and light-dependent behavior inDrosophila.Proc. Natl. Acad. Sci. 68:2669–2673.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • Hall, J. C. (1978b). Courtship among males due to male-sterile mutation inDrosophila melanogaster.Behav. Genet. 8:125–141.

    PubMed  Google Scholar 

  • Hall, J. C. (1982). Genetics of the nervous system inDrosophila.Q. Rev. Biophys. 15:1–223.

    PubMed  Google Scholar 

  • 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 

  • Hildreth, P. E. (1965). Doublesex, a recessive gene that transforms both males and females ofDrosophila into intersexes.Genetics 51:659–678.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • Howard, R. W., and Blomquist, G. J. (1982). Chemical ecology and biochemistry of insect hydrocarbons.Annu. Rev. Entomol. 27:149–172.

    Google Scholar 

  • 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 

  • 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 

  • Jallon, J.-M., and Hotta, Y. (1979). Genetic and behavioral studies of female sex-appeal inDrosophila.Behav. Genet. 8:487–502.

    Google Scholar 

  • Jallon, J.-M., and Hotta, Y. (1980). A proposal for sex-appealless mutant hunting.Dros. Inform. Serv. 55:65.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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.

  • Jeffcoat, R. (1979). The biosynthesis of unsaturated fatty acids and its control in mammalian liver.Essays Biochem. 15:1–36.

    PubMed  Google Scholar 

  • Katase, H., and Chino, H. (1982). Transport of hydrocarbons by the lipophorin of insect hemolymph.Biochim. Biophys. Acta 710:341–348.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • Leahy, M. G. (1966). Egg deposition inD. melanogaster increased by transplant of male paragonia.Dros. Inform. Serv. 41:45.

    Google Scholar 

  • Leopold, R. (1976). The role of male accessory glands in insect reproduction.Annu. Rev. Entomol. 199–221.

  • Luyten, I. (1982). Variations intraspécifiques et interspécifiques des hydrocarbures cuticulaires chezDrosophila simulans C.R. Acad. Sci. Paris 295:723–736.

    Google Scholar 

  • 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 

  • McRobert, S., and Tompkins, L. (1983). Courtship of young males is ubiquitous inDrosophila melanogaster.Behav. Genet. 13:517–523.

    PubMed  Google Scholar 

  • 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 

  • Manning, A. (1959a). The sexual behaviour of two siblingDrosophila species.Behaviour 15:123–145.

    Google Scholar 

  • Manning, A. (1959b). The sexual isolation betweenD. melanogaster andD. simulans.Anim. Behav. 7:60–65.

    Google Scholar 

  • Manning, A. (1967). The control of sexual receptivity in femaleDrosophila melanogaster.Anim. Behav. 15:239–250.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Merrell, D. J. (1949). Selective mating inDrosophila melanogaster.Genetics 34:370–389.

    Google Scholar 

  • 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 

  • 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 

  • Nissani, N. (1977). Gynandromorph analysis of some aspects of sexual behavior ofDrosophila melanogaster.Anim. Behav. 5:351–366.

    Google Scholar 

  • 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 

  • 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).

  • Postlewaith, J. M., and Handler, A. (1978). Nonvitellogenic female sterile mutants and the regulation of vitellogenesis inDrosophila melanogaster.Dev. Biol. 67:202–213.

    PubMed  Google Scholar 

  • Richmond, R., Gilbert, D., Sheehan, K., Gromko, M., and Butterworth, F. (1980). Esterase 6 and reproduction inDrosophila melanogaster.Sciences 207:1483–1485.

    Google Scholar 

  • Robertson, H. M. (1983). Chemical stimuli eliciting courtship by males inD. melanogaster.Experientia 39:333–335.

    Google Scholar 

  • Rodrigues, V., and Siddiqi, O. (1978). Genetic analysis of chemosensory pathway.Proc. Ind. Acad. Sci. 87B;147–160.

    Google Scholar 

  • 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 

  • 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 

  • Shorey, H. H. (1976).Animal communication by pheromones Academic Press, New York.

    Google Scholar 

  • Shorey, H., and Bartell, R. (1970). Role of a volatile sex pheromone in stimulating male courtship behaviour inDrosophila melanogaster.Anim. Behav. 18:159–164.

    PubMed  Google Scholar 

  • 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 

  • Spence, G. E., Hoffmann, A. A., and Parsons, P. A. (1984). Habitat marking, males attracted to residual odours of twoDrosophila species.Experientia (in press).

  • Spieth, H. (1974). Courtship behavior inDrosophila.Annu. Rev. Entomol. 19:385–405.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • Sturtevant, A. (1915). Experiments on sex recognition and the problem of sexual selection inDrosophila.J. Anim. Behav. 5:351–366.

    Google Scholar 

  • 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 

  • Tompkins, L., and Hall, J. C. (1981b).Drosophila males produce a pheromone which inhibits courtship.Z. Naturforsch. 36c:694–695.

    Google Scholar 

  • 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 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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 

  • 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 

  • Venard, R., and Jallon, J.-M. (1980). Evidence for an aphrodisiac pheromone of femaleDrosophila.Experientia 36:211–212.

    Google Scholar 

  • 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 

  • von Schilcher, F. (1976). The role of auditory stimuli in the courtship ofDrosophila melanogaster.Anim. Behav. 24:18–26.

    Google Scholar 

  • 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 

  • Wigglesworth, V. B. (1974).Insect Physiology, Chapman and Hall, London.

    Google Scholar 

  • Wood, D., and Ringo, J. (1980). Male mating discrimination inD. melanogaster, D. simulans and their hybrids.Evolution 34:320–329.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jallon, JM. A few chemical words exchanged byDrosophila during courtship and mating. Behav Genet 14, 441–478 (1984). https://doi.org/10.1007/BF01065444

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01065444

Key Words

Navigation