The neural circuits of animals, including humans, are the combined product of adaptation by natural selection and the evolutionary history of a species. Distinguishing which features of neural circuits represent fundamental principles of circuit design versus the quirks of a particular model species requires comparative approaches. Features of neural circuit design and architecture that have evolved independently multiple times in distantly related species indicate elements of optimal solutions to solving a particular behavioral or cognitive problem. At the same time, aspects of neural systems that have evolved to facilitate novel behavior provide key insights into the process by which neural systems can be modified while maintaining function. Here we seek funding to develop the paper wasp, Polistes fuscatus, as a model system in neuroscience. Remarkably, these wasp uses facial individual recognition to differentiate among nestmates. Like primates, these wasps use holistic visual processing of faces and show cognitive specializations for facial recognition. In many respects, paper wasp social behavior is more similar to cooperatively breeding vertebrates than other social insects like honey bees or ants. These wasps represent an independent evolution of specialized face processing relative to primates, allowing for comparisons of the architecture of neural encoding of facial identity between distantly related groups that have independently evolved eyes and facial recognition. At the same time, our recent work shows that individual recognition has evolved in paper wasps within the last few thousand years meaning that we have a rare opportunity to understand how neural circuits underlying complex social behavior have arisen from ancestral abilities. We propose a multi-pronged approach that takes advantage of modern tools in neuroscience that will allow us to rapidly begin to characterize the neural encoding of faces in wasps. (Aim 1) We will leverage our expertise in single cell genomic approaches to identify which cell types within the wasp brain are involved in facial processing and individual recognition. (Aim 2) We will build on preliminary data from multi-channel electrophysiological recordings to examine the neural encoding of facial recognition in the wasp brain. These two approaches can be readily applied to non-model species such as paper wasps and provide a direct and immediate path forward for establishing paper wasps as a model for neuroscience studies of social recognition. (Aim 3) We will work to screen and optimize viral vectors for transgene expression in paper wasps. Viral vectors of genetically encoded tools for recording and manipulating neurons are now commonplace in model and non-model vertebrates, but rare in insects. Identifying which vectors work in wasps will immediately open a wide range of possible experiments and will be readily shared with the scientific community. Paper wasps accomplish remarkably sophisticated and complex social behavior in a small brain – investing in their development as a model system will help uncover fundamental principles of neural systems governing social behavior.

Interpreting social signals is necessary for normal human social behavior and as a result understanding the fundamental principles of circuits that mediate social behavior is critical. This work seeks to develop a novel insect model system, the paper wasp, which has a small brain yet a rich set of complex social behavior, including facial individual recognition, that are not found in current neuroscience model species. This work will help reveal fundamental principles of the design and function of neural systems involved in social behavior, with implications for diseases with deficits in social interactions.