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Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones

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.

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Figure 1: Functional assay of the pgFAR E and Z alleles in yeast.
Figure 2: Segregation of the E and Z alleles of pgFAR.
Figure 3: Detection of pgFAR RNA in female pheromone glands.
Figure 4: Phylogenetic relationships of insect FARs.

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.

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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.

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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

Correspondence to Jean-Marc Lassance or Christer Löfstedt.

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The authors declare no competing financial interests.

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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

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