Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones

Abstract

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.

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Figure 1: Evolution of sex pheromone diversity and behavioural response in Nasonia parasitoid wasps.
Figure 2: Genetics of sex pheromone differences between N. vitripennis and N. giraulti males.
Figure 3: Phylogeny and dsRNA-mediated knockdown of candidate genes.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The sequences reported in this article are deposited in GenBank under accession numbers FN429934FN429952, FN430419 and HE962018HE962021.

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Acknowledgements

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.

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Authors J.B., J.D.G., J.R. and O.N. contributed equally to this work. T.S. initiated the study. J.B., J.G., J.D.G., J.R., O.N. and T.S. conceived the experiments. D.P. conducted the bioassays. C.H., J.B., J.R. and T.S. conducted the chemical analyses. A.K.J., C.H., J.B., J.D.G., J.G., N.S.M. and O.N. performed the QTL analyses and knockdown experiments. J.D.G. and O.N. performed the transcriptional analyses. J.G., J.R., O.N. and T.S. provided material and resources. O.N. was responsible for the comparative sequence analysis and took the lead in writing the manuscript. J.R., O.N. and T.S. were the main contributors to the writing of the manuscript.

Corresponding author

Correspondence to Oliver Niehuis.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

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)

Supplementary Data

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)

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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

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