Representation and modulation of social information in the ant chemosensory system

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PROJECT SUMMARY Social insects show robust and complex behaviors, and have served as important study systems in ethology for decades. However, because they are not genetically tractable, researchers have not been able to study these behaviors at the level of brain circuitry with cutting-edge neurogenetic tools. The proposed work will pioneer such tools in the clonal raider ant Ooceraea biroi, a species that uniquely combines experimental amenability with the fascinating behavior of social insects. It will then address an important biological question: how does variation in neural responsiveness give rise to consistent differences in how individuals respond to social and environmental stimuli? O. biroi is particularly suitable to study this question for a number of reasons. First, the ants reproduce asexually and clonally, implying that behavioral differences arise from phenotypic plasticity, rather than genetic differences. Second, unlike in conventional model systems like Drosophila or mice, differences in behavioral propensities are adaptive because they give rise to stable division of labor in a colony context. Accordingly, these differences are robust and predictable, and they have received a lot of theoretical and empirical attention at the behavioral level. Given that ants communicate almost exclusively via pheromones, we will focus on the antennal lobe, the primary processing area of chemosensory information in the insect brain, analogous to the mammalian olfactory bulb. In Aim 1, we will generate transgenic lines expressing the genetically encoded calcium indicator GCaMP in the antennal lobe to enable live imaging of neural activity with two-photon microscopy. We will also generate lines expressing the photoactivatable fluorescent protein CaMPARI2, enabling stable labeling of neurons active in freely behaving animals. In Aim 2, we will use these tools to create a functionally annotated map of chemosensory representation in the ant antennal lobe. We will also use single-cell RNA-sequencing of labelled neurons to identify odorant receptors responding to pheromones. We will then use the promoters of these receptors to generate additional, narrowly targeted transgenic lines. In Aim 3, we will study how differences in neural representation and sensitivity correlate with plastic differences in behavioral responses to identical social stimuli. Based on these data, we will build a predictive theoretical model of division of labor in insect societies. On a fundamental level, our results on the modulation of sensory perception will also inform our understanding of human disorders involving abnormal sensory sensitivity, such as autism and schizophrenia. Finally, we will make the tools and protocols developed under this proposal available to the scientific community, greatly advancing the field of social insect neuroscience and opening up a vast new experimental space. The robust and expansive behavioral repertoire of social insects combined with the simplicity of a compact invertebrate nervous system allows O. biroi to fill an important niche in neuroscience.