Each animal species has adapted its behaviors to its ecological niche through the course of evolution, presumably through changes in the nervous system. The current proposal aims to understand how nervous systems and behaviour evolve by using the fruit fly Drosophila sechellia, which is a powerful model system for comparative neurobiology. D.sechellia is closely-related to D. melanogaster – one of the best-understood and experimentally accessible model nervous system – but has adapted to a very different ecological niche. In contrast to the cosmopolitan generalist D. melanogaster, D. sechellia is endemic to the Seychelles archipelago, where it feeds, breeds and lays eggs on a single host plant, Morinda citrifolia. Morinda fruit emits characteristic volatile cues that attracts D. sechellia but repel D. melanogaster. Previous work in the host lab has identified methyl hexanoate as a cue which is detected by the odorant receptor OR22a and mediates long-range attraction. Importantly, both the physiological sensitivity and the number of these two classes of olfactory sensory neurons (OSNs) are increased in D. sechellia compared to D. melanogaster. However, how the peripheral signal is represented in the second-order interneurons (i.e. projection neurons; PNs), which carry olfactory information from the primary olfactory center (antennal lobe; AL) to higher brain centers (mushroom body and lateral horn), has not been characterized, precluding an appreciation of how these olfactory circuits evoke different types of behavior and the nature of evolutionary adaptations in the central brain.
By comparative calcium imaging of olfactory neurons in D. melanogaster and D. sechellia, I found that OSN sensitization is correlated to PN sensitization while OSN number increase itself is not. Rather, OSN number increase is correlated to sustainment of PN activity in response to dynamic odour inputs. PAGFP labelling revealed that the PN number was not different between species despite the increase in their cognate OSN number, suggesting an increased pooling of OSN inputs per PN. Optogenetic activation of Or22a OSNs elicited attractive behaviour in both species, but the duration of which was more sustained in D. sechellia. Taken together, these results imply that evolutionary increase of OSN number underlies robust tracking of odour plumes by sustaining the PN activity through increased pooling, thereby promoting host adaptation in D. sechellia.
The evolution of the nervous system is a topic of high public interest, as it is closely related to the question on the emergence of human brain and intelligence. The current proposal aimed to understand how the central olfactory circuitry has evolved to give rise to species-specific behaviors, by developing and applying neuroanatomical and neurophysiological analyses in a non-model organism, D. sechellia. The results from this project would be of general interest not only in the field of neuroscience but also evolution, ecology, and genetics.
