Sex pheromones play a pivotal role in the communication of many sexually reproducing organisms1. Accordingly, speciation is often accompanied by pheromone diversification enabling proper mate finding and recognition2. Current theory implies that chemical signals are under stabilizing selection by the receivers who thereby maintain the integrity of the signals3. How the tremendous diversity of sex pheromones seen today evolved is poorly understood4,5. Here we unravel the genetics of a newly evolved pheromone phenotype in wasps and present results from behavioural experiments indicating how the evolution of a new pheromone component occurred in an established sender–receiver system. We show that male Nasonia vitripennis evolved an additional pheromone compound differing only in its stereochemistry from a pre-existing one. Comparative behavioural studies show that conspecific females responded neutrally to the new pheromone phenotype when it evolved. Genetic mapping and gene knockdown show that a cluster of three closely linked genes accounts for the ability to produce this new pheromone phenotype. Our data suggest that new pheromone compounds can persist in a sender’s population, without being selected against by the receiver and without the receiver having a pre-existing preference for the new pheromone phenotype, by initially remaining unperceived. Our results thus contribute valuable new insights into the evolutionary mechanisms underlying the diversification of sex pheromones. Furthermore, they indicate that the genetic basis of new pheromone compounds can be simple, allowing them to persist long enough in a population for receivers to evolve chemosensory adaptations for their exploitation.
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.
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 Ch. 3 37–73 (Cambridge Univ. Press, 2003)
Smadja, C. & Butlin, R. K. On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102, 77–97 (2009)
Butlin, R. K. & Trickett, A. J. in Insect Pheromone Research: New Directions (eds Cardé, R. T. & Minks, A. K. ) 548–562 (Chapman & Hall, 1997)
Symonds, M. R. E. & Elgar, M. A. The evolution of pheromone diversity. Trends Ecol. Evol. 23, 220–228 (2008)
Steiger, S., Schmitt, T. & Schaefer, H. M. The origin and dynamic evolution of chemical information transfer. Proc. R. Soc. B 278, 970–979 (2011)
Roelofs, W. L. & Rooney, A. P. Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc. Natl Acad. Sci. USA 100, 9179–9184 (2003)
Ferveur, J.-F. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav. Genet. 35, 279–295 (2005)
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)
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)
Lassance, J.-M. et al. Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466, 486–489 (2010)
Liénard, M. A., Hagström, A. K., Lassance, J.-M. & Löfstedt, C. Evolution of multicomponent pheromone signals in small ermine moths involves a single fatty-acyl reductase gene. Proc. Natl Acad. Sci. USA 107, 10955–10960 (2010)
Albre, J. et al. Sex pheromone evolution is associated with differential regulation of the same desaturase gene in two genera of leafroller moths. PLoS Genet. 8, e1002489 (2012)
Werren, J. H. & Loehlin, D. W. The parasitoid wasp Nasonia: an emerging model system with haploid male genetics. Cold Spring Harb. Protocols 2009, pdb.emo134 (2009)
Werren, J. H. et al. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327, 343–348 (2010)
Ruther, J., Stahl, L. M., Steiner, S., Garbe, L. A. & Tolasch, T. A male sex pheromone in a parasitic wasp and control of the behavioral response by the female’s mating status. J. Exp. Biol. 210, 2163–2169 (2007)
Ruther, J., Steiner, S. & Garbe, L.-A. 4-Methylquinazoline is a minor component of the male sex pheromone in Nasonia vitripennis . J. Chem. Ecol. 34, 99–102 (2008)
Abdel-latief, M., Garbe, L. A., Koch, M. & Ruther, J. An epoxide hydrolase involved in the biosynthes is of an insect sex attractant and its use to localize the production site. Proc. Natl Acad. Sci. USA 105, 8914–8919 (2008)
Steiner, S. & Ruther, J. Mechanism and behavioral context of male sex pheromone release in Nasonia vitripennis . J. Chem. Ecol. 35, 416–421 (2009)
Munoz-Torres, M. C. et al. Hymenoptera Genome Database: integrated community resources for insect species of the order Hymenoptera. Nucleic Acids Res. 39, D658–D662 (2011)
Niehuis, O. et al. Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia . PLoS ONE 5, e8597 (2010)
Punta, M. et al. The Pfam protein families database. Nucleic Acids Res. 40, D290–D301 (2012)
Tanner, M. E. Understanding nature’s strategies for enzyme-catalyzed racemization and epimerization. Acc. Chem. Res. 35, 237–246 (2002)
Kavanagh, K. L., Jörnvall, H., Persson, B. & Oppermann, U. Medium- and short-chain dehydrogenase/reductase gene and protein families: the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell. Mol. Life Sci. 65, 3895–3906 (2008)
Cho, H., Oliveira, M. A. & Tai, H.-H. Critical residues for the coenzyme specificity of NAD+-dependent 15-hydroxyprostaglandin dehydrogenase. Arch. Biochem. Biophys. 419, 139–146 (2003)
Niehuis, O., Judson, A. K. & Gadau, J. Cytonuclear genic incompatibilities cause increased mortality in male F2 hybrids of Nasonia giraulti and N. vitripennis . Genetics 178, 413–426 (2008)
Broman, K. W., Wu, H., Sen, S. & Churchill, G. A. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19, 889–890 (2003)
Niehuis, O., Büllesbach, J., Judson, A. K., Schmitt, T. & Gadau, J. Genetics of cuticular hydrocarbon differences between males of the parasitoid wasps Nasonia giraulti and Nasonia vitripennis . Heredity 107, 61–70 (2011)
Lynch, J. A. & Desplan, C. A method for parental RNA interference in the wasp Nasonia vitripennis . Nature Protocols 1, 486–494 (2006)
Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011)
We thank J. H. Werren for providing laboratory strains of Nasonia and Trichomalopsis and D. Wheeler for discussion on the gene expression data. G. Amdam and J. Liebig allowed us to use their research facilities for conducting the gene expression studies, knockdown experiments and gas chromatography analyses. We thank D. D. McKenna and R. S. Peters for comments on an earlier draft of this paper. O.N. acknowledges the Alexander von Humboldt foundation for a Feodor Lynen postdoctoral research stipend. J.B. and T.S. were supported by the Excellence Initiative of the German Research Foundation (GSC-4, Spemann Graduate School). Parts of this research were supported by the German Research Foundation (DFG) grant RU 717/10-1 to J.R.
The authors declare no competing financial interests.
This file contains Supplementary Methods (Species and strains, Comparative chemical analysis, Preparation of enantiopure HDL stereoisomers, Behavioural bioassays, QTL and fine mapping, Introgression experiments, Gene knockdown experiments, Gene expression analysis, Rapid Amplification of cDNA ends (RACE), Comparative nucleotide and amino acid sequence analysis), Supplementary Data (Introgression experiments, Possible functions of NV10124, NV10126, NV10130 and NV30591, Annotation of putative SDR-coding genes in candidate region, Comparative nucleotide and amino acid sequence analysis), Supplementary References, Supplementary Tables 1–5 and Supplementary Figures 1–5. (PDF 452 kb)
This file contains additional Supplementary Data showing the detailed annotation of the putative SDR-coding candidate genes NV10127, NV10128 and NV10129. The annotations are provided in a file as plain text in generic feature format (.gff). (TXT 3 kb)
About this article
Cite this article
Niehuis, O., Buellesbach, J., Gibson, J. et al. Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones. Nature 494, 345–348 (2013). https://doi.org/10.1038/nature11838
Proceedings of the National Academy of Sciences (2020)
Journal of Chemical Ecology (2020)
Philosophical Transactions of the Royal Society B: Biological Sciences (2020)
Evolutionary Ecology (2020)
Detection of very long-chain hydrocarbons by laser mass spectrometry reveals novel species-, sex-, and age-dependent differences in the cuticular profiles of three Nasonia species
Analytical and Bioanalytical Chemistry (2019)