Abstract
Recent results from biochemical and molecular genetic studies of the accessory gland proteins in maleDrosophila are reviewed. The most prominent feature is the species-specific variability. However, the analysis of the sex peptide inD. melanogaster shows that there is a strong homology in the molecular structure to the closely related sibling species, and that divergence increases with increasing phylogenetic distance. For this reason the sex peptide, after being transferred to the female genital tract during copulation, reduces receptivity and increases oviposition only in virgin females belonging to the same species group and subgroup. Even though studies were hitherto limited to a small number of the secretory components, it is evident that the accessory gland proteins play a key role in reproductive success of the fruit fly by changing female sexual behavior, supporting sperm transfer, storage and displacement. Thus, genes encoding the accessory gland proteins are apparently under strong evolutionary selection.
Similar content being viewed by others
References
Aguadè, M., Miyashita, N., and Langley, C., Polymorphism and divergence in theMst26a male accessory gland gene region inDrosophila. Genetics132 (1992) 755–770.
Aigaki, T., Fleischmann, I., Chen, P. S., and Kubli, E., Ectopic expression of sex peptide alters reproductive behavior of femaleD. melanogaster. Neuron7 (1991) 557–563.
Bairati, A., Structure and ultrastructure of the male reproductive system inD. melanogaster Meig. 2. The genital duct and accessory glands. Monit. Zool. Ital. (NS)2 (1968) 105–182.
Baumann, H., The isolation, partial characterization and biosynthesis of the paragonial substances PS-1 and PS-2 ofD. funebris. J. Insect Physiol.20 (1974) 2181–2194.
Baumann, M., Wilson, K. J., Chen, P. S., and Humbel, R. E., The amino-acid sequence of a peptide (PS-1) fromDrosophila funebris: A paragonial peptide from males which reduces the receptivity of the females. Eur. J. Biochem.52 (1975) 521–529.
Betram, M. J., Akerkar, G. A., Gonzàlez, C., and Wolfner, M. F., Cell type-specific gene expression in theDrosophila melanogaster male accessory gland. Mech. Dev.38 (1992) 33–40.
Bixler, A., Jenkins, J. B., Tompkins, L., and McRobert, S. P., Identification of acoustic stimuli that mediate sexual behavior inDrosophila buskii (Diptera: Drosophilidae). J. Insect Behav.5 (1992) 469–478.
Bownes, M., and Patridge, L., Transfer of molecules from ejaculate to famales inDrosophila pseudoobscura. J. Insect Physiol.33 (1987) 941–947.
Burnet, B., and Connolly, K., Activity and sexual behaviour inDrosophila melanogaster, in: The Genetics of Behaviour, pp. 201–258. Ed. J. H. F. van Abeelen, North Holland 1974.
Chapman, T., Liddle, L., Kalb, J., Wolfner, M. F., and Patridge, L., Cost of mating inDrosophila melanogaster females is mediated by male accessory gland products. Nature373 (1995) 241–244.
Chen, P. S., Species-specific patterns inDrosophila paragonial glands. Experientia32 (1976) 549–550.
Chen, P. S., The functional morphology and biochemistry of insect male accessory glands and their secretions. A. Rev. Ent.29 (1984) 233–255.
Chen, P. S., Biochemistry and molecular regulation of the male accessory gland secretions inDrosophila (Diptera). Annls Soc. ent. Fr. (N.S.)27 (1991) 231–244.
Chen, P. S., and Balmer, J., Secretory proteins and sex peptide of the male accessory gland inDrosophila sechellia. J. Insect Physiol.35 (1989) 759–764.
Chen, P. S., Stumm-Zollinger, E., and Caldelari, M., Protein metabolism ofDrosophila male accessory glands—II. Species-specificity of secretion proteins. Insect Biochem.15 (1985) 385–390.
Chen, P. S., Stumm-Zollinger, E., Aigaki, T., Balmer, J., Bienz, M., Böhlen, P., A male accessory gland peptide that regulates reproduc-tive behavior of femaleD. melanogaster. Cell54 (1988) 291–298.
Clark, A. G., Silveria, S., Meyers, W., and Langley, C. H., Nature screen: an efficient method for screening natural populations ofDrosophila for P-element insertion. Proc. natl Acad. Sci. USA91 (1994) 719–722.
Clark, A. G., Aguadè, M., Prout, T., Harshman, L. G., and Langley, C. H., Variation in sperm displacement and its association with accessory gland protein loci inDrosophila melanogaster. Genetics139 (1995) 189–201.
David, J., Influence de la fecondation de la femelle sur le numbre et la taille des oeufs pondus. J. Insect Physiol.9 (1963) 13–24.
DiBenedetto, A. J., Harada, H. A., and Wolfner, M., Structure, cell-specific expression, and mating induced regulation of aDrosophila melanogaster male accessory gland gene. Devl Biol.139 (1990) 134–148.
Fleischmann, I., Dauwalder, B., Chapman, T., Cotton, B., and Kubli, E., Thedunce gene product might be physiologically involved in sex-peptide response inDrosophila melanogaster. (Abstract S12-11). Experientia51 (1995) A59.
Fowler, G. L., Some aspects of the reproductive biology ofDrosophila: Sperm transfer, sperm storage and sperm utilization. Adv. Genet.17 (1973) 293–360.
Gillott, C., Arthropoda—Insecta, in: Reproductive Biology of Invertebrate, vol. 3: Accessory Sex Glands, pp. 319–471. Eds K. G. Adiyodi and R. G. Adiyodi. John Wiley & Sons, Chichester 1988.
Gonzàlez, A. M., Cabrera, V. M., Larruga, J. M., and Guillo, A., Genetic distance in the sibling speciesDrosophila melanogaster, Drosophila simulans andDrosophila mauritiana. Evolution36 (1982) 517–522.
Hadorn, E., Zur Autonomie und Phasenspezifität der Letalität von Bastarden zwischenDrosophila melanogaster andDrosophila simulans. Rev. suisse zool.68 (1961) 197–207.
Happ, G. M., Structure and development of male accessory glands in insects, in: Insect Ultrastructure, vol. 2, pp. 365–398. Eds. R. C. King, and H. Aki. Plenum Press, New York 1984.
Harris, M. O., and Miller, J. R., Quantitative analysis of ovipositional behavior: effects of a host plant chemical on the onion fly (Diptera: Anthomyiidae). J. Insect Behavior4 (1991) 773–792.
Harshman, L. G., and Prout, T., Sperm displacement without sperm transfer inDrosophila melanogaster. Evolution48 (1994) 753–766.
Ito, Y., and Yamagishi, M., Sperm competition in the melon fly,Dacus cucurbitae (Diptera: Tephritidae): Effects of sequential matings with normal and virgin or non-virgin sterile males. Appl. Ent. Zool.24 (1989) 466–477.
Jallon, J. M., Laugè, G., Orssaud, L., and Antony, C., Female pheromones inDrosophila melanogaster are controlled by the doublesex locus. Genet. Res.51 (1988) 17–22.
Kalb, J. M., DiBenedetto, A. J., and Wolfner, M., Probing the function ofDrosophila melanogaster accessory glands by directed cell ablation. Proc. natl Acad. Sci. USA90 (1993) 8093–8097.
Knipling, E. F., The Basic Principles of Insect Population Suppression and Management. U.S. Department of Agriculture, Agriculture Handbook No. 512, Washington, D.C. (cited from Spencer et al.57).
Kubli, E., My favorite molecule: the sex peptide. BioEssays.14 (1992) 779–784.
Kubli, E., TheDrosophila sex-peptide: A peptide pheromone involved in reproduction, in: Advances in Developmental Biochemistry, vol. 4, pp. 99–128. Ed. P. Wassermann. JAl Press Inc. USA 1996.
Lamb, M. J., The effect of radiation on the longevity of femaleDrosophila subobscura. J. Insect Physiol.10 (1964) 487–489.
Lemeunier, F., and Ashburner, M., Relationships within themelanogaster species group of the genusDrosophila (Sophophora). II. Phylogenetic relationship between six species based upon polytene chromosome banding sequences. Proc. R. Soc., London,193 (1976) 275–294.
Lemeunier, F., and Ashburner, M., Relationships within themelanogaster species subgroup of the genusDrosophila (Sophophora). IV. The chromosomes of two new species. Chromosoma89 (1984) 343–351.
Lindsley, D. L., and Zimm, G. G., The Genome ofDrosophila melanogaster. Academic Press, San Diego, California 1992.
Luckinbill, L. S., Arking, R., Clare, M. J., Cirocco, W. C., and Buck, S. A., Selection of delayed senescence inDrosophila melanogaster. Evolution38 (1984) 996–1003.
Manning, A., A sperm factor affecting the receptivity ofDrosophila melanogaster females. Nature194 (1962) 252–253.
Markow, T. A., and Ankney, P. F.,Drosophila males contribute to oogenesis in multiple mating species. Science224 (1984) 302–303.
Menn, J. J., and Hollingworth, R. M., Insect control, 1. Introduction, in: Comparative Insect Physiology, Biochemistry and Pharmacology, vol. 12, pp. 1–8. Eds. G. A. Kerkut and L. I. Gilbert. Pergamon Press, Oxford 1985.
Moshitzky, P., Fleischmann, I., Saudan, P., Klauser, S., Kubli, E., and Applebaum, S. W., Sex-peptide activates juvenile hormone biosynthesis in theDrosophila melanogaster corpus allatum. Archives of Insect Biochemistry and Physiology, vol. 32. Wiley-Liss Inc. USA 1996.
Mosma, S. A., and Wolfner, M., Structure and expression of aDrosophila male accessory gland gene whose product resembles a peptide pheromone precursor. Genes Dev.2 (1988) 1063–1073.
Mosma, S. A., Harada, H. A., and Wolfner, M., Synthesis of twoDrosophila male accessory gland proteins and their fate after transfer to the female during mating. Dev. Biol.142 (1990) 465–475.
Ohashi, Y. Y., Haino-Fukushima, K., and Fuyama, Y., Purification and characterization of an ovulation stimulating substance from the male accessory gland ofDrosophila suzukii. Insect Biochem.21 (1991) 413–419.
Osanai, M., Aigaki, T., Kasuga, H., and Yonezawa, Y., Role of arginase transferred from the vesicula seminalis during mating and changes in amino acid pools of the spermatophore after ejaculation in the silkworm,Bombyx mori. Insect Biochem.16 (1986) 879–885.
Patridge, L., Fowler, K., Trevitt, S., and Sharp, W., An examination of the effects of males on the survival and egg-production rates of femaleDrosophila melanogaster. J. Insect Physiol.32 (1986) 925–929.
Patridge, L., Green, A., and Fowler, K., Effects of egg-production and of exposure to males on female survival inDrosophila melanogaster. J. Insect Physiol.33 (1987) 745–749.
Reding, T. V., Proteinmuster der Paragoniendrüsen von Hybridmännchen der SchwesterartenDrosophila melanogaster undDrosophila simulans. Diplomarbeit, Universität Zürich 1985.
Rose, M. R., Laboratory evolution of postpond senescence inDrosophila melanogaster. Evolution38 (1984) 1004–1010.
Rosen, D., Biological control, in: Comprehensive Insect Physiology, Biochemistry and Pharmacology, vol. 12, Insect Control, 414–464. Eds G. A. Kerkut and L. I. Gilbert. Pergamon Press, Oxford 1985.
Schmidt, T., Stumm-Zollinger, and Chen, P. S., Protein metabolism ofDrosophila melanogaster male accessory gland—III. Stimulation of protein synthesis following copulation. Insect Biochem.15 (1985) 391–401.
Schmidt, T., Stumm-Zollinger, E., Chen, P. S., Böhlen, P., and Stone, S. R., A male accessory gland peptide with protease inhibitory activity inDrosophila funebris. J. biol. Chem.264 (1989) 9745–9749.
Schmidt, T., Choffat, Y., Klauser, S., and Kubli, E., TheDrosophila melanogaster sex peptide: a molecular analysis of structure-function relationships. J. Insect Physiol.39 (1993a) 361–368.
Schmidt, T., Choffat, Y., Schneider, M., Hunziker, P., Fumaya, Y., and Kubli, E.,Drosophila suzukii contains a peptide homologous to theDrosophila melanogaster sex-peptide and functional in both species. Insect Biochem. Molec. Biol.23 (1993b) 571–579.
Spencer, J. L., Bush, G. L., Keller, J. E., and Miller, J. R., Modification of female onion fly,Delia antiqua (Meigen) reproductive behavior by paragonial gland extracts (Diptera: Anthomyiidae). J. Insect Behavior5 (1992) 689–697.
Stumm-Zollinger, E., and Chen, P. S., Protein metabolism ofDrosophila male accessory glands.—I. Characterization of secretory proteins. Insect Biochem.15 (1985) 375–383.
Stumm-Zollinger, E., and Chen, P. S., Gene expression of male accessory glands of interspecific hybrids ofDrosophila. J. Insect Physiol.34 (1988) 59–74.
Styger, D., Molekulare Analyse des Sexpeptidgens ausDrosophila melanogaster. Ph. D. Thesis, University of Zürich, Zürich 1992.
Szabad, J., and Fajszi, C., Control of female reproduction inDrosophila: Genetic dissection of using gynandromorphs. Genetics100 (1989) 61–78.
Thornhill, R., and Alcock, J., The Evolution of Insect Mating Systems. Harvard University Press, Cambridge, Mass. and London 1983.
Tompkins, L., Genetic analysis of sex appeal inDrosophila. Behav. Genetics14 (1984) 411–440.
Tompkins, L., Genetic control of sexual behavior inDrosophila melanogaster. Trends Gen. (TIG)2 (1986) 14–17.
Tompkins, L., The development of male- and female-specific sexual behavior inDrosophila melanogaster, in: Genetics of Development and Evolution. Eds R. N. Chatterjee and P. Gergen, in press.
Tompkins, L., and Hall, J. C., Identification of brain sites controlling female receptivity in mosaics ofDrosophila melanogaster. Genetics103 (1983) 179–195.
Wahlen, M., and Wilson, T. G., Variation and genomic localization of genes encodingDrosophila melanogaster male accessory gland proteins separated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Genetics114 (1986) 77–92.
Wehner, R., and Gehring, W., Zoologie. Geor Thieme Verlag, Stuttgart and New York 1990.
Wolfner, M. F., Tokens of love: function and regulation ofDrosophila male accessory gland products. Insect Biochem. and molec. Bio. (in preparation).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Chen, P.S. The accessory gland proteins in maleDrosophila: structural, reproductive, and evolutionary aspects. Experientia 52, 503–510 (1996). https://doi.org/10.1007/BF01969718
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01969718