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Macroglomeruli for fruit odors change blend preference in Drosophila

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Abstract

The olfactory circuitry of Drosophila melanogaster is becoming increasingly clear. However, how olfactory processing translates into appropriate behavioral responses is still poorly understood. Using a sibling species approach, we tested how a perturbation in the olfactory circuitry affects odor preference. In a previous study, we found that the sibling species of D. melanogaster, the specialist D. sechellia, overrepresents a sensillum, ab3, the A neuron of which is sensitive to hexanoate esters, characteristic of the species’ sole host, the Morinda citrifolia fruit. Concordantly, the corresponding glomerulus, DM2, is enlarged. In this study, we found that the ab3B neuron, the expansion of which was previously assumed to be pleiotropic and of no ecological significance, is in fact tuned to another morinda fruit volatile, 2-heptanone (HP). Axons of this neuron type arborize in a second enlarged glomerulus. In behavioral experiments we tested how this has affected the fly’s odor preference. We demonstrate that D. sechellia has a reversed preference for the key ligands of these macroglomeruli, especially at high concentrations. Whereas D. melanogaster was repelled by high concentrations of these odors, D. sechellia was highly attracted. This was the case for odors presented singly, but more notably for blends thereof. Our study indicates that relatively simple changes, such as a shift in sensillar abundance, and concordant shifts in glomerular size, can distort the resulting olfactory code, and can lead to saltatory shifts in odor preference. D. sechellia has exploited this to align its olfactory preference with its ecological niche.

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Acknowledgements

The authors thank G. Stemmler of the GoodNoni company Fiji Islands for shipments of morinda fruit. The study was funded through the Linnaeus grant, ICE3, to the division of Chemical Ecology, Alnarp Sweden, FORMAS grant 2007–1491 to TD, and by MIUR, International Interuniversity Cooperation to AMA.

Authors’ contributions

I. Ibba performed the experiments, analysed the data and drafted the manuscript. T. Dekker conceived the concept of the study and contributed to interpretation of data and writing the manuscript. A.M. Angioy and B. Hansson were involved in interpretation of data and writing of the manuscript. All authors have read and approved the final version of the manuscript.

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Authors and Affiliations

  1. Department of Experimental Biology, Section of General Physiology, University of Cagliari, SS 554 Km 4.5, Monserrato, Italy

    Irene Ibba & Anna Maria Angioy

  2. Division of Chemical Ecology, Swedish University of Agricultural Sciences, PO Box 102, 23053, Alnarp, Sweden

    Irene Ibba & Teun Dekker

  3. Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Hans Knoell Strasse 8, 07745, Jena, Germany

    Irene Ibba & Bill S. Hansson

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  1. Irene Ibba
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  2. Anna Maria Angioy
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Correspondence to Teun Dekker.

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Ibba, I., Angioy, A.M., Hansson, B.S. et al. Macroglomeruli for fruit odors change blend preference in Drosophila . Naturwissenschaften 97, 1059–1066 (2010). https://doi.org/10.1007/s00114-010-0727-2

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  • DOI: https://doi.org/10.1007/s00114-010-0727-2

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