Abstract
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, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Accession codes
Primary accessions
GenBank/EMBL/DDBJ
Data deposits
The sequences reported in this article are deposited in GenBank under accession numbers FJ807735–FJ807736, GU808256–GU808276 and GU733831–GU733832.
References
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)
Acknowledgements
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.
Author information
Authors and Affiliations
Contributions
J.M.L., A.T.G., D.G.H. and C.L. performed project design and interpretation. J.M.L., M.A.L. and B.A. conducted cloning of pgFAR cDNAs. F.A. and E.H. were responsible for the synthesis of precursors. J.M.L. and M.A.L. performed the functional assays. J.M.L. conducted the gas chromatography–mass spectrometry analyses. A.T.G., C.B. and D.G.H. performed QTL analyses and gene mapping. D.G.H. was responsible for the genomic sequence analysis. J.M.L. performed the transcriptional analysis. J.M.L. was responsible for bioinformatics. J.M.L., A.T.G., M.A.L., D.G.H. and C.L. prepared the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Methods, References, Supplementary Figures 1-5 with legends and Supplementary Tables 1-3. (PDF 578 kb)
Rights and permissions
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature09058
This article is cited by
-
Release of moth pheromone compounds from Nicotiana benthamiana upon transient expression of heterologous biosynthetic genes
BMC Biology (2022)
-
Rapid divergence of a gamete recognition gene promoted macroevolution of Eutheria
Genome Biology (2022)
-
bric à brac controls sex pheromone choice by male European corn borer moths
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)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.