CAREER: Transcriptional Regulation of Piezo2 Channels in a Behavioral and Evolutionary Context

The sense of touch is fundamental to the lived experience of all animals, including humans. In vertebrates, the ability to convert physical force into an electrical signal that the brain interprets as touch relies on the ion channel Piezo2. Understanding how Piezo channels are developmentally regulated and discovering the differences in their function in species with diverse touch sensation are the focus of this investigation. The investigators will compare waterfowl species that have evolved to possess a finely honed sense of touch with those that do not, to reveal mechanisms of how neurons become touch-sensitive during development and the evolution of molecules that are critical for touch. This research will provide useful tools for studying touch, adding an important and overlooked layer of sensory information that will aid in understanding how these species use their habitats, and thus aid in their conservation. The project will enable training of scientists at multiple career stages in integrative research methods through funded research and course-based research activities. These activities seamlessly integrate into planned outreach at the Lexington Public Library (LPL), designed to teach critical vocational skills and increase scientific literacy and engagement from the broader community. In addition, the team will partner with LPL, Sylvan Heights Bird Park, and Prepared Minds lab and Advanced Robotics lab to bring about methodological and conceptual advances for the understanding of touch and waterfowl ecology. Currently, Piezo2 is the only verified mechanically gated ion channel known to transduce touch in vertebrate somatosensory neurons. While touch is important in an organismal/evolutionary context, how Piezo2 is transcriptionally regulated is unknown. Thus, there is a critical need to determine how Piezo2 is regulated both on developmental and evolutionary timescales. To accomplish this, investigators will leverage a novel clade of model organisms: ducks (Anatidae). Many species of duck are expert “tactile foragers,” using sense of touch in their bill which is innervated by trigeminal ganglia (TG) neurons to feed. The percentage of Piezo2 positive neurons expressed in duck TG varies widely in species with differing foraging behavior, suggesting Piezo2 is differentially regulated across species. Investigators will identify regulatory elements for Piezo2 using multiomics in TG neurons at developmental timepoints spanning the onset of Piezo2 expression and experimentally validate promoters/enhancers using in ovo electroporation of reporter constructs. This study will then characterize a second axis of Piezo2 regulation—its role in the evolution of sensory specialization by correlating Piezo2 expression, functional mechanosensitivity, and variation in regulatory elements in duck species with disparate mechanosensory abilities. Finally, Course-Based Undergraduate Research courses will refine and extend novel behavioral assays for quantifying tactile ability in ducks, with the immediate goal of determining the extent of behavioral species diversity in tactile foraging, and long-term goal of testing manipulations of Piezo2. This project is jointly funded by Organization/Neural Systems Cluster and the Established Program to Stimulate Competitive Research (EPSCoR). This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.