Skip to main content
Log in

Relations Between Cuticular Hydrocarbon (HC) Polymorphism, Resistance Against Desiccation and Breeding Temperature; A Model for HC Evolution in D. Melanogaster and D. Simulans

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

D. simulans and D. melanogaster present two types of polymorphism in their cuticular hydrocarbon (HC) composition. Especially both sexes of D. simulans, and D. melanogaster males display 7-tricosene (7T) as the major compound type [7T]s and [7T]m, or 7-pentacosene (7P) [7P]s and [7P]m. D. melanogaster females display 7,11-heptacosadiene (7,11HD) as the major compound: [7,11HD]m, or 5,9-heptacosadiene (5,9HD): [5,9HD]m. The [7P]s, [7P]m and [5,9HD]m are mainly present in central Africa. A significant correlation was found between latitude and the proportion of compounds with 23 and 25 carbon atoms, especially 7T and 7P in both sexes of D. melanogaster. [7P]m type of D. melanogaster, characterized with an excess of C25 compounds, presents a higher resistance against desiccation than [7T]m type, where C23 compounds are more abundant. These differences can be correlated with calculated HC fusion temperatures. Moreover, increasing the breeding temperature from 18 to 29°C induces in D. melanogaster males an increase in 25C compounds and a decrease in 23C compounds, but the opposite effect in D. simulans. A mathematical model of biosynthesis, based on kinetics of elongation and decarboxylation enzymes, suggests that a simple variation of the efficiency of an elongation enzyme may account for the differences observed between the [7T]m and [7P]m types of D. melanogaster and [7T]s and [7P]s types D. simulans. Finally on the basis of the geographical distribution of the HC types of both Drosophila species, an evolutionary dispersal pathway is proposed and discussed in relation to the environment and reproductive behavior.

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

  • Antony, C. & J.-M. Jallon, 1981. Evolution des hydrocarbures comportementalement actifs de Drosophila melanogaster au cours de la maturation sexuelle. Comptes rendus de l'Académie des Sciences de Paris, Série III t292: 239–242.

    Google Scholar 

  • Antony, C. & J.-M. Jallon, 1982. The chemical basis for sex recognition in Drosophila melanogaster. J. Insect Physiol. 28: 873–880.

    Google Scholar 

  • Antony, C., T.L. Davis, D.A. Carlson, J.M. Péchiné & J.-M. Jallon, 1985. Compared behavioral responses of male Drosophila melanogaster (Canton S) to natural and synthetic aphrodisiacs. J. Chem. Ecol. 11: 1617–1629.

    Google Scholar 

  • Arienti, M., 1993. Analyse de la variabilité de quelques mécanismes impliqués dans le comportement sexuel de populations différentes de Drosophila melanogaster. Thèse de doctorat de l'Université Paris XI Orsay, France, 217 pp.

  • Blomquist, G.L., J.W. Dillwith & T.S. Adams, 1987. Biosynthesis and endocrine regulation of sex pheromone production in Diptera, pp. 217–250 in Pheromone Biochemistry, edited by G.D. Prestwich & G.J. Blomquist. Academic Press, London.

    Google Scholar 

  • Carlson, D.A., M.S. Mayer, D.L. Silhacek, D. James, M. Beroza & B.A. Birl, 1971. Sex attractant pheromone of the house fly: isolation, identification and synthesis. Science 174: 57–59.

    Google Scholar 

  • Chan Yong, T.P. & J.-M. Jallon, 1986. Synthèse de novo d'hydrocarbures potentiellement aphrodisiaques chez les Drosophiles. Comptes rendus de l'Académie des Sciences de Paris, Série III 303: 97–202.

    Google Scholar 

  • Cobb, M. & J.-M. Jallon, 1990. Pheromones, mate recognition and courtship stimulation in the Drosophila melanogaster sub-group. Anim. Behav. 39: 1058–1067.

    Google Scholar 

  • Coyne, J.A., C. Wicker-Thomas & J.-M. Jallon, 1999. A gene responsible for a pheromonal polymorphism in Drosophila melanogaster. Genet. Res. Camb. 73: 189–203.

    Google Scholar 

  • Dallerac, R., C. Labeur, J.-M. Jallon, D.C. Knipple, W.L. Roelofs & C. Wicker-Thomas, 2000. A 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in D. melanogaster. Proc. Natl. Acad. Sci. USA 97: 9449–9454.

    Google Scholar 

  • David, J.R. & P. Capy, 1988. Genetic variation of Drosophila melanogaster natural population. TIG 4: 106–111.

    Google Scholar 

  • Doi, M., T. Nemoto, H. Nakanishi & Y. Oguma, 1997. Behavioral response of males to major sex pheromone component, (Z,Z)-5,25-hentriacontadiene, of Drosophila ananassae. J. Chem. Ecol. 23: 2067–2078.

    Google Scholar 

  • Fang, S., A. Takahashi & C.I. Wu, 2002. A mutation in the promoter of desaturase 2 is correlated with sexual isolation between Drosophila behavioral races. Genetics 162: 781–784.

    Google Scholar 

  • Ferveur, J.-F., 1991. Genetic control of pheromones in Drosophila simulans. 1 Ngbo, a locus on the second chromosome. Genetics 128: 293–301.

    Google Scholar 

  • Ferveur, J.-F. & J.-M. Jallon, 1996. Genetic control of male cuticular hydrocarbons in Drosophila melanogaster. Genet. Res. Camb. 67: 211–218.

    Google Scholar 

  • Ferveur, J.-F. & G. Sureau, 1996. Simultaneous influence on male courtship of stimulatory and inhibitoring pheromones produced by live sex-mosaic Drosophila melanogaster. Proc. R. Soc. Lond. B 263: 967–973.

    Google Scholar 

  • Ferveur, J.-F., M. Cobb, H. Boukella & J.-M. Jallon, 1996. World wide variations in Drosophila melanogaster sex pheromone: behavioural effects, genetic bases and potential evolutionary consequences. Genetica 97: 73–80.

    Google Scholar 

  • Ferveur, J.-F., F. Savarit, C.J. O'Kane, G. Sureau, R.J. Greenspan & J.-M. Jallon, 1997. Genetic feminization of pheromones and its behavioral consequences in Drosophila males. Science 276: 1555–1558.

    Google Scholar 

  • Gibbs, A.G., 1998. Water-proofing properties of cuticular lipids. Am. Zool. 38: 471–482.

    Google Scholar 

  • Gibbs, A. & J.G. Pomonis, 1995. Physical properties of insect cuticular hydrocarbons: model mixtures and lipid interactions. Comp. Biochem. Physiol. 112B: 667–672.

    Google Scholar 

  • Gibert, P., P. Capy, A. Imasheva, B. Moreteau, J.P. Morin, G. Pétavy & J.R. David, 2004. Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica 120: 165–179.

    Google Scholar 

  • Hadley, N.F., 1978. Cuticular permeability of desert tenebrionid beetles: correlations with epicuticular hydrocarbon composition. Insect Biochem. 8: 17–22.

    Google Scholar 

  • Haerty, W., J.-M. Jallon, J.D. Rouault, C. Bazin & P. Capy, 2002. Reproductive isolation in natural populations of Drosophila melanogaster from Brazzaville (Congo). Genetica 116: 215–224.

    Google Scholar 

  • Jallon, J.-M., 1984. A few chemical words exchanged by Drosophila during courtship and mating. Behav. Genet. 14: 441–478.

    Google Scholar 

  • Jallon, J.-M. & Y. Hotta, 1979. Genetic and behavioral studies of female sex appeal in Drosophila. Behav. Genet. 9: 257–275.

    Google Scholar 

  • Jallon, J.-M. & Y. Hotta, 1981. Non chemical messages of the female Drosophila melanogaster, pp. 136-144 in Genetic Dissection of Drosophila Behavior, edited by Y. Hotta. University of Tokyo Press.

  • Jallon, J.-M. & J.M. Péchiné, 1989. Une autre race chimique de Drosophila melanogaster en Afrique. Comptes rendus de l'Académie des Sciences de Paris, Série III 309: 1551–1556.

    Google Scholar 

  • Jallon, J.-M., C. Antony & O. Benamar, 1981. Un antiaphrodisiaque produit par les males de Drosophila melanogaster et transféré aux femelles lors de la copulation. Comptes rendus de l'Académie des Sciences de Paris, Série III 292: 1147–1149.

    Google Scholar 

  • Labeur, C., R. Dallerac & C. Wicker-Thomas, 2002. Involvement of desat1 gene in the control of Drosophila melanogaster pheromone biosynthesis. Genetica 114: 269–274.

    Google Scholar 

  • Lachaise, D. & J.-F. Silvain, 2004. How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120: 17–39.

    Google Scholar 

  • Lachaise, D., M.-L. Cariou, J.R. David, F. Lemeunier, L. Tsacas & M. Ashburner, 1988. Historical biogeography of the Drosophila melanogaster species subgroup. Evol. Biol. 22: 159–225.

    Google Scholar 

  • Lachaise, D., M. Harry, M. Solignac, F. Lemeunier, V. Bénassi & M.-L. Cariou, 2000. Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé. Proc. R. Soc. Lond. B 267: 1487–1495.

    Google Scholar 

  • Lemeunier, F., S. Aulard, M. Arienti, J.-M. Jallon, M.-L. Cariou & L. Tsacas, 1997. The ercepeae complex: new cases of insular speciation within the Drosophila ananassae species subgroup (melanogaster group) and descriptions of two new species (Diptera: Drosophilidae) Ann. Entomol. Soc. of Am. 90: 28–42.

    Google Scholar 

  • Lockey, K.H., 1976. Cuticular hydrocarbons of Locusta, Schistocerca and Periplaneta, and their role in waterproofing. Insect Biochem. 6: 457–472.

    Google Scholar 

  • Luyten, I., 1982. Variation intraspécifique et interspécifique des hydrocarbures cuticulaires chez Drosophila simulans et des espèces affines. Comptes rendus de l'Académie des Sciences de Paris, Série III 295: 733–736.

    Google Scholar 

  • Nemoto, T., M. Doi, K. Oshio, H. Matsubayashi, Y. Oguma, T. Suzuki & Y. Kuwabara, 1994. (Z,Z)-5,27-tritriaconvadiene: major sex pheromone of Drosophila pallidosa (Diptera: Drosophilidae). J. Chem. Ecol. 20: 3029–3037.

    Google Scholar 

  • Oguma, Y., T. Nemoto & Y. Kuwahara, 1992a. Z-11-pentacosene is the major sex pheromone component in Drosophila virilis. Chemoecology 3: 60–64.

    Google Scholar 

  • Oguma, Y., T. Nemoto & Y. Kuwahara, 1992b. A sex pheromone study of a fruit fly Drosophila virilis Sturtevant (Diptera: Drosophilidae): additive effect of cuticular alkadienes to major sex pheromone. Appl. Entomol. Zool. 27: 499–505.

    Google Scholar 

  • Oguma, Y., J.-M. Jallon, M. Tomaru & H. Matsubayashi, 1996. Courtship behavior and sexual isolation between Drosophila auraria and D. triauraria in darkness and light. J. Evol. Biol. 9: 803–815.

    Google Scholar 

  • Péchiné, J.M., F. Perez, C. Antony & J.-M. Jallon, 1985. A further characterization of Drosophila cuticular monoenes using a mass spectrometry method to localize double bonds in complex mixtures. Anal. Biochem. 145: 177–182.

    Google Scholar 

  • Péchiné, J.M., C. Antony & J.-M. Jallon, 1988. Precise characterization of cuticular compounds in young Drosophila by mass spectrometry. J. Chem. Ecol. 14: 1071–1085.

    Google Scholar 

  • Pennanec'h, M., 1993. Etudes sur la biosynthèse des hydrocarbures cuticulaires des drosophiles. Thèse de doctorat de l'Université Paris XI Orsay, France, 173 pp.

  • Pennanec'h, M., L. Bricard, G. Kunesh & J.-M. Jallon, 1997. Incorporation of fatty acids into cuticular hydrocarbons of male and female Drosophila melanogaster. J. Insect Physiol. 43: 1111–1116.

    Google Scholar 

  • Ranz, J.M., C.I. Castillo-Davis, C.D. Meiklejohn & D.L. Hantl, 2003. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300: 1742–1745.

    Google Scholar 

  • Reed, J.R., P. Hernandez, G.J. Blomquist, R. Feyerreesen & R.C. Reitz, 1996. Hydrocarbon biosynthesis in the house fly, Musca domestica: substrate specificity and cofactor requirement of P450 hyd. Insect Biochem. Mol. Biol. 26: 267–276.

    Google Scholar 

  • Rouault, J., P. Capy & J.-M. Jallon, 2001. Variations of male cuticular hydrocarbons with geoclimatic variables: an adaptative mechanism in Drosophila melanogaster? Genetica 110: 117–130.

    Google Scholar 

  • Rybak, F., G. Sureau & T. Aubin, 2002. Functional coupling of acoustic and chemical signals in the courtship behavior of the male Drosophila melanogaster. Proc. R. Soc. Lond. B 269: 695–701.

    Google Scholar 

  • Savarit, F., G. Sureau, M. Cobb & J.-F. Ferveur, 1999. Genetic elimination of known pheromones reveals the fundamental chemical bases of mating and isolation of Drosophila. Proc. Natl. Acad. Sci. USA 96: 9015–9020.

    Google Scholar 

  • Scott, D., 1994. Genetic variation for female mate discrimination in Drosophila melanogaster. Evolution 48: 112–121.

    Google Scholar 

  • Scott, D. & L.L. Jackson, 1988. Interstrain comparison of male-predominant antiaphodisiacs in Drosophila melanogaster. J. Insect Physiol. 34: 863–871.

    Google Scholar 

  • Sureau, G. & J.-F. Ferveur, 1999. Co-adaptation of pheromone production and behavioural responses in Drosophila melanogaster males. Genet. Res. Camb. 74: 129–137.

    Google Scholar 

  • Takahashi, A., S.C. Tsaur, J. Coyne & C.I. Wu, 2001. The nucleotide changes governing cuticular hydrocarbon variation and their evolution in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98: 3920–3925.

    Google Scholar 

  • Tillman-Wall, J.A., D. Vanderwel, M.E. Kuenzli, R.C. Reitz & G.J. Blomquist, 1992. Regulation of sex pheromone biosynthesis of the house fly Musca domestica: relative contribution of the elongation and reductive step. Arch. Biochem. Mol. Biol. 28: 705–715.

    Google Scholar 

  • Tillman, J.A., S.J. Seybold, R.A. Jurenka & G.J. Blomquist, 1999. Insect pheromones: an overview of biosynthesis and endocrine regulation. Insect Biochem. Mol. Biol. 29: 481–514.

    Google Scholar 

  • Toolson, E.C., 1982. Effects of rearing temperature on cuticle permeability and epicuticular lipid composition in Drosophila pseudoobscura. J. Exp. Zool. 222: 249–253.

    Google Scholar 

  • Toolson, E.C., T.A. Markow, L.L. Jackson & R.W. Howard, 1990. Epicuticular hydrocarbon composition of wild and laboratory reared Drosophila mojavensis Patterson and Crow (Diptera: Drosophilidae). Ann. Entomol. Soc. Am. 83: 1165–1176.

    Google Scholar 

  • Vessereau, A., 1978. Sur l'intervalle de confiance d'une proportion: logique “classique” et logique “bayésienne”. Revue de Statistique Appliquée 26: 5–31.

    Google Scholar 

  • Wicker-Thomas, C., C. Henriet & R. Dallerac, 1997. Partial characterization of a fatty acid desaturase gene in Drosophila melanogaster. Insect Biochem. Mol. Biol. 27: 963–972.

    Google Scholar 

  • World Meteorological Organization, 1971. Climatological Normals (CLINO) for Climat and Climat Ship Stations for the Period 1931-1960. WMO/OMM No. 117, WMO, 2nd edn 1982.

  • Yamamoto, D., J.-M. Jallon & A. Komatsu, 1997. Genetic dissection of sexual behavior in Drosophila melanogoster. Annu. Rev. Entomol. 42: 551–585.

    Google Scholar 

  • Zawitowski, S. & R.C. Richmond, 1986. Inhibition of courtship and mating of Drosophila melanogaster by the male-produced lipid, cis-vaccenyl acetate. J. Insect Physiol. 32: 189–192.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rouault, JD., Marican, C., Wicker-Thomas, C. et al. Relations Between Cuticular Hydrocarbon (HC) Polymorphism, Resistance Against Desiccation and Breeding Temperature; A Model for HC Evolution in D. Melanogaster and D. Simulans . Genetica 120, 195–212 (2004). https://doi.org/10.1023/B:GENE.0000017641.75820.49

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:GENE.0000017641.75820.49

Navigation