Comparative analysis of behavioral and transcriptional variation underlying CO2 sensory neuron function and development in Drosophila

Carbon dioxide is an important environmental cue for many insects, regulating many behaviors including some that have direct human impacts. To further improve our understanding of how this system varies among closely related insect species, we examined both the behavioral response to CO₂ as well as the transcriptional profile of key developmental regulators of CO₂ sensory neurons in the olfactory system across the Drosophila genus. We found that CO₂ generally evokes repulsive behavior across most of the Drosophilids we examined, but this behavior has been lost or reduced in several lineages. Comparisons of transcriptional profiles from the developing and adult antennae for subset these species suggest that behavioral differences in some species may be due to differences in the expression of the CO₂ co-receptor Gr63a. Furthermore, these differences in Gr63a expression are correlated with changes in the expression of a few genes known to be involved in the development of the CO₂ circuit, namely dac, an important regulator of sensilla fate for sensilla that house CO₂ ORNs, and mip120, a member of the MMB/dREAM epigenetic regulatory complex that regulates CO₂ receptor expression. In contrast, most of the other known structural, molecular, and developmental components of the peripheral Drosophila CO₂ olfactory system seem to be well-conserved across all examined lineages. These findings suggest that certain components of CO₂ sensory ORN development may be more evolutionarily labile, and may contribute to differences in CO₂-evoked behavioral responses across species.