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Olfactory receptor and circuit evolution promote host specialization

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Khallaf,  Mohammed A.
Department of Neuroethology, Prof. B. S. Hansson, MPI for Chemical Ecology, Max Planck Society;
IMPRS on Ecological Interactions, MPI for Chemical Ecology, Max Planck Society;

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Hansson,  Bill S.
Department of Evolutionary Neuroethology, Prof. B. S. Hansson, MPI for Chemical Ecology, Max Planck Society;

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Knaden,  Markus
Research Group Dr. M. Knaden, Insect Behavior, Department of Neuroethology, Prof. B. S. Hansson, MPI for Chemical Ecology, Max Planck Society;

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Citation

Auer, T. O., Khallaf, M. A., Silbering, A. F., Zappia, G., Ellis, K., Álvarez-Ocaña, R., et al. (2020). Olfactory receptor and circuit evolution promote host specialization. Nature, 579, 402-408. doi:10.1038/s41586-020-2073-7.


Cite as: https://hdl.handle.net/21.11116/0000-0003-03C5-B
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.