Pheromone-based behaviours are crucial in animals from insects to mammals1,2, and reproductive isolation is often based on pheromone differences1,2,3,4. However, the genetic mechanisms by which pheromone signals change during the evolution of new species are largely unknown4. In the sexual communication system of moths (Insecta: Lepidoptera), females emit a species-specific pheromone blend that attracts males over long distances1,2,4. The European corn borer, Ostrinia nubilalis, consists of two sex pheromone races, Z and E, that use different ratios of the cis and trans isomers of acetate pheromone components5. This subtle difference leads to strong reproductive isolation in the field between the two races6,7, which could represent a first step in speciation. Female sex pheromone production and male behavioural response are under the control of different major genes8,9, but the identity of these genes is unknown. Here we show that allelic variation in a fatty-acyl reductase gene essential for pheromone biosynthesis accounts for the phenotypic variation in female pheromone production, leading to race-specific signals. Both the cis and trans isomers of the pheromone precursors are produced by both races, but the precursors are differentially reduced to yield opposite ratios in the final pheromone blend as a result of the substrate specificity of the enzymes encoded by the Z and E alleles. This is the first functional characterization of a gene contributing to intraspecific behavioural reproductive isolation in moths, highlighting the importance of evolutionary diversification in a lepidopteran-specific family of reductases. Accumulation of substitutions in the coding region of a single biosynthetic enzyme can produce pheromone differences resulting in reproductive isolation, with speciation as a potential end result.
This is a preview of subscription content
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Wyatt, T. D. Pheromones and Animal Behaviour: Communication by Smell and Taste (Cambridge University Press, 2003)
Wyatt, T. D. Fifty years of pheromones. Nature 457, 262–263 (2009)
Coyne, J. A. & Orr, H. A. Speciation (Sinauer Associates, 2004)
Smadja, C. & Butlin, R. K. On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102, 77–97 (2009)
Klun, J. A. et al. Insect sex pheromones: minor amount of opposite geometrical isomer critical to attraction. Science 181, 661–663 (1973)
Cardé, R. T. et al. European corn borer: pheromone polymorphism or sibling species? Science 199, 555–556 (1978)
Malausa, T. et al. Assortative mating in sympatric host races of the European corn borer. Science 308, 258–260 (2005)
Roelofs, W. L. et al. Sex pheromone production and perception in European corn borer moth is determined by both autosomal and sex-linked genes. Proc. Natl Acad. Sci. USA 84, 7585–7589 (1987)
Dopman, E. B., Bogdanowicz, S. M. & Harrison, R. G. Genetic mapping of sexual isolation between E and Z pheromone strains of the European corn borer (Ostrinia nubilalis). Genetics 167, 301–309 (2004)
Coyne, J. A., Crittenden, A. P. & Mah, K. Genetics of a pheromonal difference contributing to reproductive isolation in Drosophila . Science 265, 1461–1464 (1994)
Dallerac, R. et al. A Δ9 desaturase gene with a different substrate specificity is responsive for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster . Proc. Natl Acad. Sci. USA 97, 9449–9454 (2000)
Greenberg, A. J., Moran, J. R., Coyne, J. A. & Wu, C.-I. Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302, 1754–1757 (2003)
Shirangi, T. R., Dufour, H. D., Williams, T. M. & Carroll, S. B. Rapid evolution of sex pheromone-producing enzyme expression in Drosophila . PLoS Biol. 7, e1000168 (2009)
Ishikawa, Y. et al. Ostrinia spp. in Japan: their host plants and sex pheromones. Entomol. Exp. Appl. 91, 237–244 (1999)
Dopman, E. B., Pérez, L., Bogdanowicz, S. M. & Harrison, R. G. Consequences of reproductive barriers for genealogical discordance in the European corn borer. Proc. Natl Acad. Sci. USA 102, 14706–14711 (2005)
Kochansky, J., Cardé, R. T., Liebherr, J. & Roelofs, W. L. Sex pheromone of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae), in New York. J. Chem. Ecol. 1, 225–231 (1975)
Klun, J. A. & Maini, S. Genetic basis of an insect chemical communication system: the European corn borer. Environ. Entomol. 8, 423–426 (1979)
Hansson, B. S., Löfstedt, C. & Roelofs, W. L. Inheritance of olfactory response to sex pheromone components in Ostrinia nubilalis . Naturwissenschaften 74, 497–499 (1987)
Löfstedt, C., Hansson, B. S., Roelofs, W. L. & Bengtsson, B. O. No linkage between genes controlling female pheromone production and male pheromone response in the European corn borer, Ostrinia nubilalis Hübner (Lepidoptera; Pyralidae). Genetics 123, 553–556 (1989)
Knipple, D. C., Rosenfield, C.-L., Nielsen, R., You, K. M. & Jeong, S. E. Evolution of the integral membrane desaturase gene family in moths and flies. Genetics 162, 1737–1752 (2002)
Roelofs, W. L. et al. Evolution of moth sex pheromones via ancestral genes. Proc. Natl Acad. Sci. USA 99, 13621–13626 (2002)
Wolf, W. A. & Roelofs, W. L. Reinvestigation confirms action of Δ11-desaturases in spruce budworm moth sex pheromone biosynthesis. J. Chem. Ecol. 13, 1019–1027 (1987)
Zhu, J. W., Zhao, C. H., Bengtsson, M. & Löfstedt, C. Reductase specificity and the ratio regulation of E/Z isomers in the pheromone biosynthesis of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Insect Biochem. Mol. Biol. 26, 171–176 (1996)
Moto, K. et al. Pheromone gland-specific fatty-acyl reductase of the silkmoth, Bombyx mori . Proc. Natl Acad. Sci. USA 100, 9156–9161 (2003)
Antony, B. et al. Pheromone-gland-specific fatty-acyl reductase in the adzuki bean borer, Ostrinia scapulalis (Lepidoptera: Crambidae). Insect Biochem. Mol. Biol. 39, 90–95 (2009)
Lassance, J.-M. & Löfstedt, C. Concerted evolution of male and female display traits in the European corn borer, Ostrinia nubilalis . BMC Biol. 7, 10 (2009)
Guthrie, W. D., Dollinger, E. J. & Stetson, J. F. Chromosome studies of the European corn borer, smartweed borer, and lotus borer (Pyralidae). Ann. Entomol. Soc. Am. 58, 100–105 (1965)
Liénard, M. A., Strandh, M., Hedenström, E., Johansson, T. & Löfstedt, C. Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol. Biol. 8, 270 (2008)
Lander, E. S. et al. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174–181 (1987)
Heckel, D. G. Comparative genetic linkage mapping in insects. Annu. Rev. Entomol. 38, 381–408 (1993)
Xue, B., Rooney, A. P., Kajikawa, M., Okada, N. & Roelofs, W. L. Novel sex pheromone desaturases in the genomes of corn borers generated through gene duplication and retroposon fusion. Proc. Natl Acad. Sci. USA 104, 4467–4472 (2007)
Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599 (2007)
Librado, P. & Rozas, J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452 (2009)
Papanicolaou, A., Gebauer-Jung, S., Blaxter, M. L., Owen McMillan, W. & Jiggins, C. D. ButterflyBase: a platform for lepidopteran genomics. Nucleic Acids Res. 36, D582–D587 (2008)
Gasteiger, E. et al. ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31, 3784–3788 (2003)
Wang, J. et al. SilkDB: a knowledgebase for silkworm biology and genomics. Nucleic Acids Res. 33, D399–D402 (2005)
Katoh, K. & Toh, H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9, 286–298 (2008)
We thank R. G. Harrison for his comments and advice. This research was funded by the Swedish Research Council (VR), the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) and the Max-Planck-Gesellschaft.
The authors declare no competing financial interests.
About this article
Cite this article
Lassance, JM., Groot, A., Liénard, M. et al. Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466, 486–489 (2010). https://doi.org/10.1038/nature09058
Nature Communications (2021)
Biosynthesis of the Sex Pheromone Component (E,Z)-7,9-Dodecadienyl Acetate in the European Grapevine Moth, Lobesia botrana, Involving ∆11 Desaturation and an Elusive ∆7 Desaturase
Journal of Chemical Ecology (2021)
Comparative transcriptomics of the pheromone glands provides new insights into the differentiation of sex pheromone between two host populations of Chilo suppressalis
Scientific Reports (2020)
Journal of Chemical Ecology (2020)
Pheromone Odorant Receptor Responses Reveal the Presence of a Cryptic, Redundant Sex Pheromone Component in the European Corn Borer, Ostrinia nubilalis
Journal of Chemical Ecology (2020)