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The making of an olfactory specialist

View ORCID ProfileThomas O. Auer, View ORCID ProfileMohammed A. Khallaf, Ana F. Silbering, Giovanna Zappia, Kaitlyn Ellis, View ORCID ProfileBill Hansson, View ORCID ProfileGregory S.X.E. Jefferis, Sophie Caron, View ORCID ProfileMarkus Knaden, View ORCID ProfileRichard Benton
doi: https://doi.org/10.1101/546507
Thomas O. Auer
University of Lausanne;
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  • For correspondence: thomas.auer@unil.ch
Mohammed A. Khallaf
Max Planck Institute for Chemical Ecology;
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  • For correspondence: mkhallaf@ice.mpg.de
Ana F. Silbering
University of Lausanne;
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  • For correspondence: ana.silbering@unil.ch
Giovanna Zappia
University of Lausanne;
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  • For correspondence: giovanna.lucarelli@unil.ch
Kaitlyn Ellis
University of Utah;
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  • For correspondence: kaitlyn.ellis@utah.edu
Bill Hansson
Max Planck Institute for Chemical Ecology;
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  • For correspondence: hansson@ice.mpg.de
Gregory S.X.E. Jefferis
MRC Laboratory of Molecular Biology
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  • For correspondence: jefferis@mrc-lmb.cam.ac.uk
Sophie Caron
University of Utah;
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  • For correspondence: sophie.caron@utah.edu
Markus Knaden
Max Planck Institute for Chemical Ecology;
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  • For correspondence: mknaden@ice.mpg.de
Richard Benton
University of Lausanne;
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  • For correspondence: richard.benton@unil.ch
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Abstract

The evolution of animal behaviour is poorly understood. Despite numerous correlations of behavioural and nervous system divergence, demonstration of the genetic basis of interspecific behavioural differences remains rare. Here we develop a novel neurogenetic model, Drosophila sechellia, a close cousin of D. melanogaster that displays profound behavioural changes linked to its extreme host fruit specialisation. Through calcium imaging, we identify olfactory pathways detecting host volatiles. Mutational analysis indicates roles for individual receptors in long- and short-range attraction. Cross-species allele transfer demonstrates that differential tuning of one receptor is important for species-specific behaviour. We identify the molecular determinants of this functional change, and characterise their behavioural significance and evolutionary origin. Circuit tracing reveals that receptor adaptations are accompanied by increased sensory pooling onto interneurons and novel central projection patterns. This work links molecular and neuronal changes to behavioural divergence and defines a powerful model for investigating nervous system evolution and speciation.

Footnotes

  • http://jefferislab.org/si/auer2019

  • https://github.com/jefferis/fiji-cmtk-gui

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted February 12, 2019.
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The making of an olfactory specialist
Thomas O. Auer, Mohammed A. Khallaf, Ana F. Silbering, Giovanna Zappia, Kaitlyn Ellis, Bill Hansson, Gregory S.X.E. Jefferis, Sophie Caron, Markus Knaden, Richard Benton
bioRxiv 546507; doi: https://doi.org/10.1101/546507
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The making of an olfactory specialist
Thomas O. Auer, Mohammed A. Khallaf, Ana F. Silbering, Giovanna Zappia, Kaitlyn Ellis, Bill Hansson, Gregory S.X.E. Jefferis, Sophie Caron, Markus Knaden, Richard Benton
bioRxiv 546507; doi: https://doi.org/10.1101/546507

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