The evolution of the olfactory system

The evolution of the olfactory system


By Laia Torres Masjoan

Dr. Lucía Prieto-Godino, from the Francis Crick institute, recently ‘virtually’ visited the Centre for Developmental Neurobiology to present her research on the evolution of the olfactory system at the first virtual NEUReka! seminar (as part of the 2019/2020 NEUReka! Seminar Series).

Dr. Lucía Prieto-Godino has studied the embryonic development of the Drosophila olfactory system and the evolution of olfactory pathways in Drosophila during her PhD and Postdoc, respectively. She started her own lab at the Francis Crick Institute in 2018, in order to investigate this further. She has won numerous awards, including the FENS EJN Young Investigator Prize 2018 and the 2018 L’Oreal-UNESCO for women in science Fellowship. The exciting work of Dr. Prieto-Godino goes beyond the laboratory: she founded the Charity TReND (Teaching and Reasearch in Natural Sciences for Development) , which supports the scientific capacity across Africa and aims at running biomedical training courses, providing African universities with equipment and supporting their researchers.

During the seminar, Dr. Prieto-Godino presented her work on understanding how olfactory networks have evolved to encode the different behaviours across the animal kingdom. Her research group uses the Drosophila fly as a model due to its simplicity but also because of its similarity to the mammalian brain in encoding the sense of smell. Specifically, her group is working with a variety of drosophilids - all siblings of Drosophila Melanogaster (D. Melanogaster) that have diverged with different specialisms to different habitats within Africa. Throughout her talk, Dr. Prieto-Godino showed the wide range of techniques her lab employs to tackle evolutionary questions.

The olfactory system of the Drosophila fly is composed of the antenna, where the odours are detected by the olfactory sensory neurons (OSNs), and the antennal lobe, where the sensory information from the OSNs is processed, and the output information is sent to higher brain centres. Interestingly, each OSN expresses one type of receptor, and single OSNs can be recorded using electrophysiology to assess their response towards an odorant cue (Couto et al., 2005).

Dr. Prieto-Godino previously showed that two D. Melanogaster related species, D. Simulans and D. Sechellia, presented opposite behaviours towards hexanoic acid: while D. Sechellia has a strong preference towards it, D. Simulans are repelled. This indicates that hexanoic acid is an olfactory cue and the olfactory system in Drosophila evolved following the divergence-to-specificity principle, acquiring specific behaviours towards odours (Prieto-Godino et al., 2017). Using electrophysiology recordings, they showed that the OSNs expressing the receptor IR75b are highly active in D. Sechellia, but not in D. Simulans. By using the so-called “empty neuron” technique, eliminating an olfactory receptor of an OSN (the empty neuron) and miss-expressing a receptor of interest (which can be a mutated receptor), Dr. Prieto-Godino and colleagues identified a single amino acid in the binding domain of the receptor as the unique site responsible for the difference in the odorant-derived response (Prieto-Godino et al., 2016; 2017).

In her recently established lab, Dr. Prieto-Godino is using Drosophila larvae instead of adult flies, due to their conserved olfactory system as well as their simpler neuronal organization. The larvae olfactory system only contains 21 different OSNs, each expressing a different olfactory receptor and innervating a distinct glomerulus in the antennal lobe (Berk et al., 2016; Vogt et al., 2020). The simplicity of the larvae model allows, for instance, to do calcium imaging of all the 21 OSNs after chemical stimuli. A combination of calcium imaging techniques, behavioural experiments and electron microscopy based connectomics will allow assessment of how central circuit differences between drosophilids contribute to their behavioural differences.

All in all, Dr. Prieto-Godino showed that to understand the evolution of the olfactory neuronal networks that underlie animal behaviour, we need to study the sensory ecology (the environmental cues that species have adapted to), the structures specialized in the detection of these environmental cues (i.e. odorant receptors), the circuit wiring (how cells on the network are connected), and the genetics underlying the changes between species. With the use of the Drosophila larva models and the wide range of techniques presented in her talk, Dr. Lucía Prieto-Godino’s lab aims at building a picture of how simple nerve cell connections can generate incredibly complex and diverse behaviours.

References

Berck, M. E., Khandelwal, A., Claus, L., Hernandez-Nunez, L., Si, G., Tabone, C. J., ... & Samuel, A. D. (2016). The wiring diagram of a glomerular olfactory system. Elife, 5, e14859.

Couto, A., Alenius, M., & Dickson, B. J. (2005). Molecular, anatomical, and functional organization of the Drosophila olfactory system. Current Biology, 15(17), 1535-1547.

Prieto-Godino, L. L., Rytz, R., Bargeton, B., Abuin, L., Arguello, J. R., Dal Peraro, M., & Benton, R. (2016). Olfactory receptor pseudo-pseudogenes. Nature, 539(7627), 93-97.

Prieto-Godino, L. L., Rytz, R., Cruchet, S., Bargeton, B., Abuin, L., Silbering, A. F., ... & Benton, R. (2017). Evolution of acid-sensing olfactory circuits in drosophilids. Neuron, 93(3), 661-676.

Vogt, K., Zimmerman, D., Schlichting, M., Nunez, L. A. H., Qin, S., Malacon, K., ... & Samuel, A. (2020). Internal state configures olfactory behavior and early sensory processing in Drosophila larva. bioRxiv.

Banner image: Neurons in the Drosophila brain by eLife - licensed under CC BY 2.0

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