Skip to main content
Log in

Evolution of Cuticular Hydrocarbons of Hawaiian Drosophilidae

  • Original Research
  • Published:
Behavior Genetics Aims and scope Submit manuscript

Abstract

Hawaiian Drosophila offer an excellent model for adaptive evolution. More than 500 species are reported in Hawaiian islands, and there is considerable diversity in behavior and morphology. Such diversity is mainly driven by sexual selection. In this study qualitative and quantitative chemical compositions of cuticular hydrocarbons (CHCs) in 138 flies belonging to 27 Hawaiian Drosophila species, picture-winged and non picture-winged, were analyzed regarding sexual dimorphism, differences in saturation, branching position, and lengths of CHCs. We found significant variation in the CHC patterns. In several subgroups, new species show decreases in unsaturated hydrocarbons, and gradual increases in branched compounds, monomethylalkanes and dimethylalkanes, not commonly found in Drosophila. Moreover, branching positions gradually shifted towards internal carbons, and chain lengths increased in the new species. The long-term evolution of CHCs in the light of the recent evolutionary migration and adaptation history of Hawaiian Drosophila species along the developing archipelago was discussed.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Antony C, Davis TL, Carlson DA, Pechine JM, Jallon JM (1985) Compared behavioral responses of male Drosophila melanogaster (Canton S) to natural and synthetic aphrodisiacs. J Chem Ecol 1:1617–1629

    Article  Google Scholar 

  • Bächli, G. (2007) TaxoDros webside, current database version; http://taxodros.unizh.ch

  • Bartelt RJ, Armold M, Schaner AM, Jackson LL (1986) Comparative analysis of cuticular hydrocarbons in the D. virilis species group. Comp Biochem Physiol 83B:731–742

    Google Scholar 

  • Blomquist G, Dillwith JW, Adams TS (1987) Biosynthesis and endocrine regulation of sex pheromone roduction in Diptera. In: Prestwich GD, Blomquist GJ (eds) Pheromone biochemistry. Academic Press, New York, pp 217–250

    Google Scholar 

  • Boake CRB (2005) Sexual selection and speciation in Hawaiian Drosophila. Behav Genet 35:297–303

    Article  PubMed  Google Scholar 

  • Butterworth FM (1967) Lipids of Drosophila: a newly detected lipid in the male. Science 163:1256–1257

    Google Scholar 

  • Carlson DA, Mayer MS, Silhacek DL, James D, Beroza DM, Birl BA (1971) Sex attractant pheromone of the house fly: isolation, identification and synthesis. Science 174:57–59

    Article  Google Scholar 

  • Carlson DA, Langley PA, Hyuton P (1978) Sex pheromone of the tsetse fly: isolation, identification and synthesis of contact aphrodisiacs. Science 201:750–753

    Article  PubMed  Google Scholar 

  • Carlson DA, Offor II, El Messoussi S, Matsuyama K, Mori K, Jallon JM (1998) Sex pheromone of Glossina tachinoides: isolation, identification and synthesis. J Chem Ecol 24:1563–1575

    Article  Google Scholar 

  • Carson HL (1971) Polytene chromosome relationships in Hawaiian species of Drosophila. V. Additions to the chromosomal phylogeny of the picture-winged species. Univ TX Publ 7303:183–191

    Google Scholar 

  • Carson HL (1997) Sexual selection: a driver of genetic change in Hawaiian Drosophila. J Heredit 88:343–352

    Google Scholar 

  • Carson HL (2003) Mate choice theory and the mode of selection in sexual populations. Proc Natl Acad Sci USA 100:6584–6587

    Article  PubMed  Google Scholar 

  • Carson HL, Yoon JS (1981) Genetics and evolution of Hawaiian Drosophila. In: Ashburner M, Carson HL, Thompson JN (eds) The genetics and biology of Drosophila, vol 3. Academic Press, London, pp 97–344

    Google Scholar 

  • Chase J, Jurenka RA, Schal C, Halarnkar PP, Blomquist GJ (1990) Biosynthesis of methyl-branched hydrocarbons in the German cockroach Blatella germanica. Insect Biochem 20:149–156

    Article  Google Scholar 

  • Chertemps T (2004) Caracterisation moleculaire, fonctionnelle et comportementale des genes impliques dans la biosynthese des pheromones chez Drosophila melanogaster. These de Doctorat de l’Universite de Paris Sud, Orsay

    Google Scholar 

  • Chertemps T, Duportets L, Labeur C, Ueyama M, Wicker-Thomas C (2005) A new elongase expressed in Drosophila male reproductive system. Biochem Biophys Res Commun 333:1066–1072

    Article  PubMed  Google Scholar 

  • Chertemps T, Duportets L, Labeur C, Ueda R, Takajashi K, Saigo K, Wicker-Thomas C (2007) A female-biased expressed elongase involved in long-chain hydrocarbon biosynthesis and courtship behavior in Drosophila melanogaster. Proc Natl Acad Sci USA 104:4273–4278

    Article  PubMed  Google Scholar 

  • Cobb M, Jallon JM (1990) Pheromones, mate recognition and courtship stimulation in the Drosophila melanogaster subgroup. Anim Behav 39:1058–1067

    Article  Google Scholar 

  • Coyne JA, Crittenden AP, Mah K (1994) Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science 265:1461–1464

    Article  PubMed  Google Scholar 

  • Dillwith JW, Nelson JH, Pomonis JH, Nelson DR, Blomquist GJ (1982) A C13-NMR study of methyl-branched hydrocarbon biosynthesis in the housefly. J Biol Chem 257:11305–11314

    PubMed  Google Scholar 

  • Ferveur JF (1997) The pheromonal role of cuticular hydrocarbons in Drosophila melanogaster. Bioassays 19:353–358

    Article  Google Scholar 

  • Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35:279–295

    Article  PubMed  Google Scholar 

  • Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New York

    Google Scholar 

  • Gibbs AG (1998) Water -proofing properties of cuticular lipids. Am Zool 38:471–482

    Google Scholar 

  • Guiraudie-Capraz G, Pho DB, Jallon JM (2007) Role of the ejaculatory bulb in the biosynthesis of the male pheromone cis-vaccenyl acetate in Drosophila melanogaster. Integr Zool 2:81–91

    Article  Google Scholar 

  • Hadley NF (1978) Cuticular permeability of desert tenebrionid beetles: correlations with epicuticular hydrocarbon composition. Insect Biochem 8:17–22

    Article  Google Scholar 

  • Hodosh RJ, Keough EM, Ringo JM (1979) The morphology of the sex pheromone gland in D. grimshawi. J Morphol 161:177–184

    Article  Google Scholar 

  • Howard RW, Blomquist GJ (2005) Ecological, behavioural and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393

    Article  PubMed  Google Scholar 

  • Hoy RR, Hoikkala A, Kaneshiro KY (1988) Hawaiian courtship songs: evolutionary innovation in communication signals in Drosophila. Science 240:217–219

    Article  PubMed  Google Scholar 

  • Jallon JM (1984) A few chemical words exchanged by Drosophila during courtship and mating. Behav Genet 14:441–478

    Article  PubMed  Google Scholar 

  • Jallon JM, David JR (1987) Variations in cuticular hydrocarbons among the eight species of the Drosophila melanogaster subgroup. Evolution 41:294–302

    Article  Google Scholar 

  • Jallon JM, Wicker-Thomas C (2003) Genetic studies on pheromone production in Drosophila. In: Blomquist GJ, Vogt RG (eds) Insect pheromone biochemistry and molecular biology. Elsevier, Amsterdam, pp 253–281

    Chapter  Google Scholar 

  • Kambysellis MP, Ho KF, Craddock E, Piano F, Parisi M, Cohen J (1995) Pattern of ecological shifts in the diversification of Hawaiian Drosophilae inferred from a molecular phylogeny. Curr Biol 5:1129–1139

    Article  PubMed  Google Scholar 

  • Kaneshiro KY (1976) Ethological Isolation and Phylogeny in the Planitibia subgroup of Hawaiian Drosophila. Evolution 30:740–745

    Article  Google Scholar 

  • Kaneshiro KY (1980) Sexual isolation, speciation, and the direction of evolution. Evolution 30:740–745

    Article  Google Scholar 

  • Kaneshiro KY (1983) Sexual selection and direction of evolution in the biosystematics of Hawaiian Drosophilidae. Ann Rev Entomol 28:161–178

    Article  Google Scholar 

  • Kondoh Y, Kaneshiro K, Kimura KI, Yamamoto D (2003) Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc R Soc Lond B 270:1005–1013

    Article  Google Scholar 

  • Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA 78:3721–3725

    Article  PubMed  Google Scholar 

  • Lande R, Kirkpatrick M (1988) Ecological speciation by sexual selection. J Theor Biol 133:85–98

    Article  PubMed  Google Scholar 

  • Langley PA, Carlson DA (1983) Biosynthesis of contact pheromones in the female tsetse fly, Glossina Morsitans. J Insect Physiol 29:825–831

    Article  Google Scholar 

  • Liimatainen J, Jallon JM (2007) Genetic analysis of cuticular hydrocarbons and their effect on courtship in Drosophila virilis and D. lummei. Behav Genet 37:713–725

    Article  PubMed  Google Scholar 

  • Lucas C, Pho DB, Fresneau D, Jallon JM (2004) Hydrocarbon circulation and colonial signature in Pachycondyla villosa. J Insect Physiol 50:595–607

    Article  PubMed  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge

    Google Scholar 

  • Nelson DR, Blomquist GJ (1995) Insect waxes. In: Hamilton RJ (ed) Chemistry, molecular biology, functions. Oily Press, Dundee, Scotland, pp 1–90

    Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • Ringo JM (1977) Why 300 species of Hawaiian Drosophila? The sexual selection hypothesis. Evolution 31:694–696

    Article  Google Scholar 

  • Ringo JM, Hodosh RJ (1978) A multivariate analysis of behavioural divergence among closely related species of endemic Hawaiian Drosophila. Evolution 32:389–397

    Article  Google Scholar 

  • Rouault JD, Marican C, Wicker-Thomas C, Jallon JM (2004) Relations between cuticular hydrocarbons, temperature breeding and resistance against desiccation: an evolution model for D. melanogaster and D. simulans. Genetica 120:195–212

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Scott D, Jackson LL (1988) Interstrain comparison of male predominant aphrodisiacs in Drosophila melanogaster. J Insect Physiol 34:863–871

    Article  Google Scholar 

  • Spieth HT (1952) Mating behavior within the genus Drosophila (Diptera). Bull Am Museum Nat History 99:401–473

    Google Scholar 

  • Spieth HT (1966) Courtship behavior of endemic Hawaiian Drosophila. Univ TX Publ 6615:245–313

    Google Scholar 

  • Spieth HT (1987) Courtship patterns and evolution of Drosophila adiastola and Drosophila planitibia species subgroups. Evolution 32:435–451

    Article  Google Scholar 

  • Thockmorton LH (1966) The relationships of the endemic Hawaiian Drosophilidae. Univ TX Publ 6615:335–396

    Google Scholar 

  • Thomas RH, Hunt JA (1993) Phylogenetic relationships in Drosophila: a conflict between molecular and morphological data. Mol Biol Evol 10:362–374

    PubMed  Google Scholar 

  • Tompkins L, McRobert SP, Kaneshiro KY (1993) Chemical communication in Hawaiian Drosophila. Evolution 47:1407–1419

    Article  Google Scholar 

  • Toolson EC (1982) Effects of rearing temperature on cuticle permeability and epicuticular lipid-composition in Drosophila pseudoobscura. J Exp Zool 222:249–253

    Article  Google Scholar 

  • Ueyama M, Chertemps T, Labeur C, Wicker-Thomas C (2005) Mutations in the desat1 gene reduces the production of courtship stimulatory pheromones through a marked effect on fatty acids in Drosophila melanogaster. Insect Biochem Mol Biol 35:911–920

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are very grateful to Dr. Ken Kaneshiro for his help with fly identifications. We thank Wolfgang Miller and John Ringo for very helpful comments on an earlier version of the manuscript. D.Y. was supported by Specially Promoted Research Grant 1802012 from the Ministry of Education, Culture, Sport, Sciences and Technology (MEXT).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jean-Marc Jallon.

Additional information

Edited by Lee Ehrman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alves, H., Rouault, JD., Kondoh, Y. et al. Evolution of Cuticular Hydrocarbons of Hawaiian Drosophilidae. Behav Genet 40, 694–705 (2010). https://doi.org/10.1007/s10519-010-9364-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10519-010-9364-y

Keywords

Navigation