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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 S. 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
1Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015, Lausanne, Switzerland
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  • For correspondence: Richard.Benton@unil.ch Thomas.Auer@unil.ch
Mohammed A. Khallaf
2Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, D-07745, Jena Germany
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Ana F. Silbering
1Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015, Lausanne, Switzerland
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Giovanna Zappia
1Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015, Lausanne, Switzerland
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Kaitlyn Ellis
3Department of Biology, University of Utah, Salt Lake City, Utah, 84112, USA
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Bill S. Hansson
2Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, D-07745, Jena Germany
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Gregory S.X.E. Jefferis
4Division of Neurobiology, MRC Laboratory of Molecular Biology, Cambridge, CB2 0QH, UK
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  • ORCID record for Gregory S.X.E. Jefferis
Sophie Caron
3Department of Biology, University of Utah, Salt Lake City, Utah, 84112, USA
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Markus Knaden
2Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, D-07745, Jena Germany
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Richard Benton
1Center for Integrative Genomics, Faculty of Biology and Medicine, University of Lausanne, CH-1015, Lausanne, Switzerland
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  • ORCID record for Richard Benton
  • For correspondence: Richard.Benton@unil.ch Thomas.Auer@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.

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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 S. 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 S. 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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