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.
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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
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
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
Boake CRB (2005) Sexual selection and speciation in Hawaiian Drosophila. Behav Genet 35:297–303
Butterworth FM (1967) Lipids of Drosophila: a newly detected lipid in the male. Science 163:1256–1257
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
Carlson DA, Langley PA, Hyuton P (1978) Sex pheromone of the tsetse fly: isolation, identification and synthesis of contact aphrodisiacs. Science 201:750–753
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
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
Carson HL (1997) Sexual selection: a driver of genetic change in Hawaiian Drosophila. J Heredit 88:343–352
Carson HL (2003) Mate choice theory and the mode of selection in sexual populations. Proc Natl Acad Sci USA 100:6584–6587
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
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
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
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
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
Cobb M, Jallon JM (1990) Pheromones, mate recognition and courtship stimulation in the Drosophila melanogaster subgroup. Anim Behav 39:1058–1067
Coyne JA, Crittenden AP, Mah K (1994) Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila. Science 265:1461–1464
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
Ferveur JF (1997) The pheromonal role of cuticular hydrocarbons in Drosophila melanogaster. Bioassays 19:353–358
Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35:279–295
Fisher RA (1958) The genetical theory of natural selection, 2nd edn. Dover, New York
Gibbs AG (1998) Water -proofing properties of cuticular lipids. Am Zool 38:471–482
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
Hadley NF (1978) Cuticular permeability of desert tenebrionid beetles: correlations with epicuticular hydrocarbon composition. Insect Biochem 8:17–22
Hodosh RJ, Keough EM, Ringo JM (1979) The morphology of the sex pheromone gland in D. grimshawi. J Morphol 161:177–184
Howard RW, Blomquist GJ (2005) Ecological, behavioural and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393
Hoy RR, Hoikkala A, Kaneshiro KY (1988) Hawaiian courtship songs: evolutionary innovation in communication signals in Drosophila. Science 240:217–219
Jallon JM (1984) A few chemical words exchanged by Drosophila during courtship and mating. Behav Genet 14:441–478
Jallon JM, David JR (1987) Variations in cuticular hydrocarbons among the eight species of the Drosophila melanogaster subgroup. Evolution 41:294–302
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
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
Kaneshiro KY (1976) Ethological Isolation and Phylogeny in the Planitibia subgroup of Hawaiian Drosophila. Evolution 30:740–745
Kaneshiro KY (1980) Sexual isolation, speciation, and the direction of evolution. Evolution 30:740–745
Kaneshiro KY (1983) Sexual selection and direction of evolution in the biosystematics of Hawaiian Drosophilidae. Ann Rev Entomol 28:161–178
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
Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA 78:3721–3725
Lande R, Kirkpatrick M (1988) Ecological speciation by sexual selection. J Theor Biol 133:85–98
Langley PA, Carlson DA (1983) Biosynthesis of contact pheromones in the female tsetse fly, Glossina Morsitans. J Insect Physiol 29:825–831
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
Lucas C, Pho DB, Fresneau D, Jallon JM (2004) Hydrocarbon circulation and colonial signature in Pachycondyla villosa. J Insect Physiol 50:595–607
Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge
Nelson DR, Blomquist GJ (1995) Insect waxes. In: Hamilton RJ (ed) Chemistry, molecular biology, functions. Oily Press, Dundee, Scotland, pp 1–90
Oguma YT, Nemoto T, Kuwahara Y (1992a) Z-11-pentacosene is the major sex pheromone component in Drosophila virilis. Chemoecology 3:60–64
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
Ringo JM (1977) Why 300 species of Hawaiian Drosophila? The sexual selection hypothesis. Evolution 31:694–696
Ringo JM, Hodosh RJ (1978) A multivariate analysis of behavioural divergence among closely related species of endemic Hawaiian Drosophila. Evolution 32:389–397
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
Scott D (1994) Genetic variation for female mate discrimination in Drosophila melanogaster. Evolution 48:112–121
Scott D, Jackson LL (1988) Interstrain comparison of male predominant aphrodisiacs in Drosophila melanogaster. J Insect Physiol 34:863–871
Spieth HT (1952) Mating behavior within the genus Drosophila (Diptera). Bull Am Museum Nat History 99:401–473
Spieth HT (1966) Courtship behavior of endemic Hawaiian Drosophila. Univ TX Publ 6615:245–313
Spieth HT (1987) Courtship patterns and evolution of Drosophila adiastola and Drosophila planitibia species subgroups. Evolution 32:435–451
Thockmorton LH (1966) The relationships of the endemic Hawaiian Drosophilidae. Univ TX Publ 6615:335–396
Thomas RH, Hunt JA (1993) Phylogenetic relationships in Drosophila: a conflict between molecular and morphological data. Mol Biol Evol 10:362–374
Tompkins L, McRobert SP, Kaneshiro KY (1993) Chemical communication in Hawaiian Drosophila. Evolution 47:1407–1419
Toolson EC (1982) Effects of rearing temperature on cuticle permeability and epicuticular lipid-composition in Drosophila pseudoobscura. J Exp Zool 222:249–253
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
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).
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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
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DOI: https://doi.org/10.1007/s10519-010-9364-y